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MEAT
SCIENCE
Meat Science 78 (2008) 114129
www.elsevier.com/locate/meatsci

Decontamination technologies for meat products


T. Aymerich, P.A. Picouet *, J.M. Monfort
IRTA, Finca Camps i Armet, E-17121 Monells, Girona, Spain
Received 9 March 2007; received in revised form 4 July 2007; accepted 9 July 2007

Abstract
Consumers demand high quality, natural, nutritious, fresh appearance and convenient meat products with natural avour and taste
and an extended shelf-life. To match all these demands without compromising safety, in the last decades alternative non-thermal preservation technologies such as HHP, irradiation, light pulses, natural biopreservatives together with active packaging have been proposed
and further investigated. They are ecient to inactivate the vegetative microorganisms, most commonly related to food-borne diseases,
but not spores. The combination of several non-thermal and thermal preservation technologies under the so-called hurdle concept has
also been investigated in order to increase their eciency. Quick thermal technologies such as microwave and radiofrequency tunnels or
steam pasteurization bring new possibilities to the pasteurization of meat products especially in ready to eat meals. Their application
after nal packaging will prevent further cross-contamination during post-processing handling. The benets of these new technologies
and their limitations in an industrial application will be presented and discussed.
2007 Elsevier Ltd. All rights reserved.
Keywords: Non-thermal and thermal technologies; Meat; Irradiation; High hydrostatic pressure; Biopreservation and natural antimicrobials; Active
packaging; Radio frequency and microwave heating; Ohmic heating; Steam pasteurization

1. Introduction
Meat is a rich nutrient matrix that provides a suitable
environment for proliferation of meat spoilage microorganisms and common food-borne pathogens, therefore adequate preservation technologies must be applied in order
to preserve its safety and quality. Food safety is a top priority
for authorities and consumers worldwide. Food safety objectives and hazard analysis and critical control point are being
introduced worldwide. In the European Union an extensive
hygienic legislative package is now into force (European Parliament & of the Council, 2002, 2004a, 2004b, 2004c, 2004d)
and the established Microbiological criteria (European
Commission, 2005a, 2005b) must be accomplished.
Nevertheless, the prevalence of food-borne pathogens
and the reported number of cases and outbreaks is still
high, thus aecting personal lives, business and countries
economies. In Europe 2005, 380,000 European Union citi*

Corresponding author. Tel.: +34 972 63 0052; fax: +34 972 63 0373.
E-mail address: pierre.picouet@irta.es (P.A. Picouet).

0309-1740/$ - see front matter 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.meatsci.2007.07.007

zens were aected by infectious zoonotic diseases, 5311


food-borne outbreaks were reported involving 47,251 people and resulting in 5330 hospitalizations and 24 deaths.
Campylobacter and Salmonella reported the highest number of cases, 197,363 and 176,395, mainly related to fresh
poultry meat and eggs, poultry and pig meat, respectively.
Yersinia enterocolitica reported 9630 cases and Escherichia
coli VTEC caused 3314 cases, which were mainly associated to fresh bovine meat. Listeria monocytogenes reported
1439 cases, mainly related to RTE products, and Brucella
mellitensis accounted for 1218 cases (European Food
Safety Authority, 2006).
Consumer demands high quality, convenient, innovative, regular and safe meat products with natural avour
and taste and an extended shelf-life. Moreover less salty,
less acidied and less chemical preserved products are
required. To match all these demands without compromising safety, the production and manufacture of meat products is at stage of innovative dynamics thus stimulating a
major research issue to develop and implement alternative
technologies such as the so called non-thermal technologies

T. Aymerich et al. / Meat Science 78 (2008) 114129


25

2002
2003
Irradiated Food in 1000xTons

or alternative, quicker, sensory-milder thermal technologies. Some promising non-thermal and thermal technologies are being considered at industrial level for
decontamination of meat products, gamma, electron and
X-ray irradiation, high hydrostatic pressure (HHP), natural antimicrobials, active packaging, ohmic heating, microwave and radiofrequency and steam among others. All
these alternative technologies try to be mild, guarantee natural appearance, energy saving and environmentally
friendly while knocking the pathogens and spoilage microorganisms. Their combination, as in the hurdle theory proposed by Leistner (2000) may improve their eectiveness.

20

2004
2005

15

10

Total

MRCM

The irradiation technology implies the exposure of meat


products to ionizing irradiation to decontaminate food
products. It was rst suggested in 1897, 1-year after Roetgens discovered X-rays and it was patented in England in
1905. From 1940 to 1960, research was conducted at the
quartermaster laboratory of the US Army to provide sterilized cans to the US army. In 1962, the rst food irradiation facility was built for the army and the USDA issued
the rst food irradiation rules in 1963 to decontaminate
wheat and wheat powder (Ahn, Lee, & Mendonca, 2006).
The rst meat irradiation rules were published by the
USDA in 1985 to inactivate Trichinella spiralis in pork carcass and in 1997, the irradiation of red ground meat was
authorized. It was promoted by the FAO in the Codex Alimentarius in 2003 and was well accepted in 50 countries,
especially in USA, Latin America, Egypt and China. In
Europe, consumer acceptance has postponed its application and irradiation of food is restricted to dried aromatic
herbs, spices and vegetable seasoning (European Parliament & of the Council, 1999a, 1999b). Although on the
approximation of National laws of the member states,
the EU commission has authorised the treatment of meat
products in some countries (European Commission,
2001). Fig. 1 shows the amount of irradiated meat products
treated in dierent European countries from 2002 to 2005.
Ionizing irradiation occurs when one or more electrons
are removed from the electronic orbital of the atom. It
can be produced by three dierent techniques (Table 1),
gamma ray processing, high energy electron called e-beam
and X-ray processing. Gamma rays are mainly produced
by a source of radionuclides, Cobalt 60 with a half life of
5.27 years and Cesium 137 with a half life of 30.19 years.
In the industry, the majority of facilities use the Cobalt
60 because it has stronger gamma ray and because it is
not soluble in water (Ahn et al., 2006). Electron beams
are produced by commercial electron accelerators and
therefore can be switch o like all electrical apparatus.
They can be directly used for small items such as grains
or to remove surface contamination because they have limited penetration capacity. X-rays are produced when fast-

Poultry

Meat

Frog Legs

Others

Products

2. Non-thermal alternative technologies


2.1. Irradiation

115

Fig. 1. The use of irradiation in Europe: Quantities (in thousand tonnes)


of irradiated products declare by four members states (Belgium, France,
Germany and Holland) to the European commission from 2002 to 2005.
Data extract from European Commission reports (COM 69, 2004, C230/
07, 2006; C230/08, 2006; C122/03, 2007). MRCM: Mechanically recovered
chicken meat.

Table 1
Summary of the depth and eciency from three ionised-irradiation
technologies used in food processing (extract from Koutchma, 2006)

Power source (kW)


Source energy (MeV)
Processing speeda (tonnes/h)
Penetration depth (cm)
Dose uniformity ratio
Dose rate (kGy/h)
a

Gamma ray

X-ray

E-beam

50
1.33
12
80100
1.7
Low

25
5
10
80100
1.5
High

35
510
510
810
Moderate
High

Processing speed to deliver a dose rate of 4 kGy.

moving electrons slam into a metal object. If the target


used is tantalum or platinum, strong X-ray with an energy
superior to 1 MeV can be produced (Table 1). The USFDA and the European Commission approved the use of
X-ray technology with a maximum energy of 5 MeV, and
then the FDA amended the maximum level to reach
7.5 MeV in 2004. The technique oers the possibility of
processing packaged meat products in great quantities
(Borsa, 2006) although it requires a high investment and
maintenance cost. Food irradiation facilities must be
designed and constructed in order to ensure the control
of the radiological hazard for the personal and the environment. Costly reinforced concrete walls must be built
around the main source and the treatment area. Additionally, the operational costs are also high. In some countries
the same amount of money can be spent on quality controls and in good hygiene practice.
The molecular bonds in the microbial DNA are the
main target of irradiation but DNA and RNA synthesis,
denaturation of enzymes and cell membrane alterations
may also be aected. The absorbed dose, measured in grays
(Gy). 1 Gy = J/kg = 100 rad, is considered the most important parameter but eectiveness of the treatment also
depends on the sensitivity of the microorganims, the extrin-

116

T. Aymerich et al. / Meat Science 78 (2008) 114129

sic characteristic of the environment (pH, temperature) and


the intrinsic characteristics of the food (fat content, salt,
additives, etc.). In general, viruses are the most resistant
to irradiation, followed by spores and yeast. Molds and
Gram-positive vegetative bacteria are more resistant than
Gram-negative. Low activity water and low temperature
promote resistance while presence of oxygen enhances the
irradiation action. Cross-adaptation to other stress as acid
has to be considered (Ahn et al., 2006; Borsa, 2006;
Koutchma, 2006; Sommers, Fan, Handel, & Sokorai,
2003).
In the food sector, irradiation is dened by two processes, radiation pasteurization (radurization), which refers
to the inactivation of non-spore bacteria with a low
absorbed dose requirement (110 kGy) and the sterilization
irradiation (radapperdization) to ensure the elimination of
Clostridium botulinum. For the last one the dose required
(European Commission, 2003a; Koutchma, 2006; McCleery & Rowe, 2002) is well above (between 40 and
50 kGy) the one permitted for commercial food (10 kGy).
A maximum dosage of 10 kGy represents a low amount
of energy (equivalent to the one needed to raise water temperature 2.4 C); this is why the technology is considered
non-thermal, thus preserving the freshness, the nutritional
quality of the meat and meat products when comparing
with thermal methods (Ahn et al., 2006). During the radurization treatment an insignicant loss of thiamine (one of
the most sensitive vitamins) is reported (Graham, Stevenson, & Steward, 1998) but changes in sensorial and colour
characteristics of the product may occur. In aerobic conditions, brown or greenish colour of fresh meat may appear
and in anaerobic packaging, an increase of the red colour
has been reported (Ahn et al., 2006; Brewer, 2004). On vacuum packaged dry cured loins and dry cured ham, Carrasco, Tarrega, Ramrez, Mingoarranz, and Cava (2005) and
Cava, Tarrega, Ramrez, Mingoarranz, and Carrasco
(2005), respectively, described an important colour change
on samples irradiated with a dose rate of 5 kGy. To solve
the problem, several techniques like pre-slaughter feeding
of antioxidants to livestock, the addition of antioxidants
extract from rosemary and onions (Nan et al., 2007) and
modied gas atmosphere packaging have been suggested
(Brewer, 2004). Oxidation of lipids may create free radicals
(Giroux & Lacroix, 1998), breakdown of triglycerides may

form 2-alkylcyclobutanes (used as a marker for irradiation


in EU) that has been reported to present potential health
risks (Marchioni et al., 2004). Characteristic odours
regardless of the degree of lipid oxidation and o-odour
from sulphur bridges proteins breakdown have also been
reported (Ahn & Lee, 2006; Ahn, Nam, Du, & Jo, 2001).
The eciency of the irradiation in meat products and
ready to eat meals (RTE) has been proven and it has been
reported in a series of reviews and articles (Ahn et al., 2006;
Farkas, 1998; Sommers, Fan, Niemira, & Rajkowski,
2004). Irradiation may eectively control the presence of
all the main food-borne pathogens such as E. coli
O157:H7, L. monocytogenes, S. aureus, Salmonella spp.
(Table 2) and Trichinella spiralis, also yeast and mould
are eectively eliminated from meat and meat products.

2.2. High hydrostatic pressure


In high hydrostatic pressure (HHP) treatment, also
known as ultra high pressure (UHP) treatments or High
pressure processing (HPP), the packaged food is placed
in the pressure vessel and submitted to water pressures
from 100 to 900 MPa. The pressure applied is isostatically
transmitted (Pascals law and Le Chatellier principle) inside
the pressure vessel; the food is compressed independently
of the product size and geometry because transmission of
pressure to the core is not mass/time dependent and thus
the process is minimized. A process of 500600 MPa may
take 2.5 min to charge 5 min for pressurization and 3 min
to discharge. The treatment could also be considered a
non-thermal process as the adiabatic heating is only 3 C
for each 100 MPa, thus representing an increment of
15 C for a 600 MPa (6000 bar, 87,000 psi) treatment.
Commercial equipments with a capacity of 10300 l are
available and can be purchased from Nicolas Correa
Hyperbaric (Spain), Stanstead Fluid Power (UK) and
Avure Technologies (USA).
Even if HHP has been recognized for microorganisms
inactivation since Hite (1899), the rst commercial food
products (jellies and jams) appeared in Japan in 1990.
Nowadays, there are some companies all over the world
(Japan, USA, Italy, Spain, Germany and Australia) using
this technology in meat products. Commercial cooked

Table 2
Eciency of irradiation in meat products
Microorganism

Source

Dose rate for 5 log10 reduction

Reference

L. monocytogenes in RTE meat mealsa


E. coli (KCTC) in marinated beef rib
Salmonella spp. in rabbit meat
FBPb in cured dry ham
FBPb in loins
FBPb in RTE meal mealsc

Gamma
Gamma
Gamma
E-beam

2.453.75 kGy
3.0 kGy
3.0 kGy
5.05.4 kGy

Gamma

1.83.0 kGy

Sommers et al. (2004)


Jo et al. (2004)
Bard (2005)
Cava et al. (2005)
Carrasco et al. (2005)
Sommers and Boyd (2006)

a
b
c

Frankfurter, bologna pasta, ham and deli turkey meat.


E. coli O157:H7, L. monocytogenes, S. aureus, and Salmonella spp.
Frankfurter, beef cheeseburger and vegetarian cheeseburg.

T. Aymerich et al. / Meat Science 78 (2008) 114129

ham, cured ham, some precooked meals with turkey and


delicatessen (sausage tapas), chicken and pork cuts, precooked meals with poultry, cooked and cured ham, Parma
ham, mortadella, bacon, salami and other smoked or not
smoked sausages are available in the market. Generally a
treatment of 600 MPa during 210 min is considered.
Although initial investment is high, the processing cost
has been estimated on 14 eurocent/kg of product treated
at 600 MPa, including investment and operation costs
(Anon., 2002). The technology is well accepted in Europe
as an alternative technology. Baron et al. (1999) reported
a 67% of acceptability from consumers of three dierent
European countries (France, Germany and United Kingdom). As for production, on commercial equipment of
300 l, a 4.51 cycles/h could be done and products treated
by HHP do not need to be labelled in USA.
As a consequence of the le Chatelier principle, HHP
produces denaturalization or modication of the proteins,
inactivation of enzymes, changes in the substrateenzyme
interactions and in carbohydrates and fats (Butz & Tauscher, 2002). The hydrophobic and electrostatic interactions are the most aected but not the hydrogen bonds
which stabilizes a-helical and b-pleated sheets (Heremans,
2001). Thus, the nutritional value, vitamins and the majority of small substances responsible for the avours of the
products are kept. This is viewed as an important benet
for the food industry (Hoover, Metrick, Papineau, Farkas,
& Knorr, 1989; Smelt, 1998; Tellez, Ramrez, Perez, Vazquez, & Simal, 2001) since minimal modications in the
sensorial characteristics of the product are introduced,
especially in cooked and cured meat products. Non-significant changes have been observed in cured ham treated at
450 MPa (Morales, Calzada, & Nunez, 2006) and in cured
and cooked ham treated at 600 MPa during 6 min at 30 C
(Garriga, Gre`bol, Aymerich, Monfort, & Hugas, 2004).
Saccani, Parolari, Tanzi, and Rabbuti (2004) reported that
a treatment of 600 MPa during 9 min did not aect the typical maturated taste of dry cured ham but it changed colour
(slight discoloration) and saltiness (enhanced perception),
the eect being inversely related to the age of the ham.
Moreover, colour changes due to oxidation of ferrous myoglobin and fat oxidation have also been reported in fresh
and marinated meat (Carlez, Rosec, Richard, & Cheftel,
1993; Cheftel & Culioli, 1997; Hugas, Garriga, & Monfort,
2002). Hugas, Garriga, and Monfort (2002) reported that
the overall physico-chemical composition of marinated
beef loin, cooked ham and dry cured ham was not signicantly aected after a treatment of 600 MPa during
10 min at 30 C The non-proteic nitrogen fraction and aminoacid content were equivalent while only a small decrease
in phosphate content on dry cured ham was detected. Fatty
acid composition and cholesterol content was kept, only x6
increased its stability in marinated beef loin and cholesterol
oxidation was reduced by lowering the 7-ketocholesterol
levels. Contents of vitamins from group B were not modied. Mineral composition was similar, only a decrease in
the calcium content was observed on cooked ham and an

117

increase in the iron content of beef loin, probably due to


a release form heme and non-heme complexes. Concerning
the bioavailability of nutrients, an increase in the solubility
of cytoplasmatic proteins was observed while the myobrillar fraction decreased, although not to the same extent as
cooking procedures.
HHP kills or sublethally injures cells by probably a combination of factors thus aecting cell membrane, cell wall,
proteins and enzymes and genetic mechanisms. Cell membrane is known to be the primary site of pressure damage
with consequent changes in the permeability of the cells,
transport systems, loss of osmotic responsiveness and incapacity to keep DpH. Cells wall and changes in cell morphology are also aected and bud scares, nodes to the
cell wall and separation of the cell wall from the membrane
have been observed by Ritz, Tholozan, Federighi, and Pilet
(2001) and Park, Sohn, Shin, and Lee (2001) with electronic microscopy. Protein denaturalization and changes
in the active centers have also been observed together with
genetic mechanisms such as replication and transcription
that are enzyme-mediated. DNA itself is highly stable
due to the a-helical is supported by hydrogen bonds. Condensation of nuclear material and increasing contact of
DNA with endonucleases have also been reported (Benito,
Ventoura, Casadei, Robinson, & Mackey, 1999; Chilton,
Isaacs, Mackey, & Stenning, 1997; Manas & Mackey,
2004; Smelt, Rijke, & Hayhurst, 1994; Wouters, Glaasker,
& Smelt, 1998). The threshold of inactivation depends on
the type of microorganism and its growth phase, the pressure applied, the time of processing, the composition of the
food, temperature, pH and activity water (Tewari, Jayas, &
Holley, 1999). Generally the Gram-negatives and cells in
growth phase are more sensitive than Gram-positives and
cells in stationary phase. Some microbial spores will need
a treatment over 1000 MPa (Kalchayanand, Sikes, Dunne,
& Ray, 1998). Eucariote vegetative forms from fungi and
molds are inactivated with pressure of 200300 MPa while
their spores need a 400 MPa treatment. High variability in
virus resistance has been described being poliovirus one of
the most resistants when compared to hepatitis A and rotavirus (Khadre & Yousef, 2002; Kingsley, Hoover, Papafragkou, & Richards, 2002). Rich nutrient media such as
meat reinforce the resistance of the microorganisms to
HHP (Hoover et al., 1989). Carbohydrates, proteins and
lipids have a protective eect (Simpson & Gilmour,
1997), thus results from buer systems could not be extrapolated to food matrices. Patterson, Quinn, Simpson, and
Gilmour (1995) reported the dierent sensitivity of L. monocytogenes and E. coli O157:H7 when treated in UHT milk,
poultry meat and buer systems. The same treatment could
reduce E. coli O157:H7 in 6 log CFU in buer while only
2.5 log in poultry meat and even less in milk. A low water
activity protects microorganisms against pressure and even
at the same aw the solute is important, in glycerol they are
more sensitive than in mono-o-disaccharide while trehalose
has a protective eect (Smelt, 1998). Moreover the cell
death increases with pressure but does not follow a rst

118

T. Aymerich et al. / Meat Science 78 (2008) 114129

order kinetics and a tail of inactivation is sometimes present (Garriga, Aymerich, Costa, Monfort, & Hugas, 2002;
Kalchayanand et al., 1998). These resistance or sublethally
injured cells could be able to grow during storage (Chen &
Hoover, 2003; Garriga, Aymerich, Costa et al., 2002; Patterson et al., 1995). Challenge test in real food matrices followed during the shelf-life of the product should be

recommended to assure the treatment is safe for any specic product to be treated (Fig. 2).
In meat products, several studies have reported the antimicrobial eect of HHP and the results obtained are summarised in Table 3. For a pasteurization purpose the
treatment considered is generally in the range of 300
600 MPa for a short period of time, from seconds to min-

12

12

HHP400
HHP600
NT 400

Log CFU/g

Log CFU/g

NT 600

15

30

45
days

60

75

90

15

30

45
days

60

75

90

Fig. 2. Behaviour of Listeria monocytogenes during storage of sliced cooked ham when stored at 6 C (a) and 1 C (b) and after being submitted (HHP) or
not (NT) to a high hydrostatic treatment of 400 and 600 MPa.
Table 3
Microbial inactivation by HHP in meat products
Target

Product

Initial counts
log (CFU/g)

Reduction
log (CFU/g)

Processa

Reference

FBPb

Meat homogenate

67

Total inactivation after


treatment

400 MPa for 10 min;


25 C

Shigehisa et al. (1991)

C. freundii

Minced beef
muscle

>5 log after treatment

300 MPa 10 min,


20 C
200 MPa 20 min,
20 C
400 MPa 20 min,
20 C

Carlez et al. (1993)

Minced beef
muscle
Raw minced meat

6.8

>4 log after 10 days (3 C)

for 20 min;

Carlez et al. (1994)

5.9

5 log after treatment

for 1 min;

Gola et al. (2000)

Mesophiles
bacteria
L. monocytogenes

MRPMc

7.3

>4 log after 15 days (2 C)

for 15 min;

Yuste et al. (2001)

Dry cured ham

2.7

for 6 min;

Salmonella spp.

Cooked ham

3.8

Aerobic total
count

Marinated beef
loin
Dry cured ham

6.5

Absence after 120 days


(4 C)
Absence after 120 days
(4 C)
>4.5 after 120 days (4 C)

450 MPa
20 C
700 MPa
15 C
450 MPa
2 C
600 MPa
31 C
600 MPa
31 C
600 MPa
31 C

Hugas, Garriga, and


Monfort (2002)
Garriga, Aymerich, and
Hugas (2002)
Garriga et al. (2004)

2.5

1.8 after 120 days (4 C)

P. uorescens
L. innocua
Total microora
E. coli O157:H7

for 6 min;
for 6 min;

L. monocytogenes
Salmonella spp.

Cooked ham

2.6
3.0

1.9 after 42 days (6 C)


2.4 after 84 days (6 C)

400 MPa for 10 min;


17 C

Aymerich et al. (2005)

L. monocytogenes

Iberian ham

6.3

3.6 after 60 days (8 C)

Morales et al. (2006)

L. monocytogenes

Sliced beef cured


ham
Ground pork
meat

4.0

2 log after 210 days (6 C)

Viable tissue cysts

Non-viable

450 MPa for 10 min;


12 C
500 MPa for 5 min;
18 C
300 MPa

Toxoplasma gondii
cysts
a
b
c

Initial temperature are reported.


E. coli, Campylobacter jejuni, Pseudomonas aeruginosa, Salmonella Typhimurium, Yersinia enterocolitica.
Mechanically recovered poultry meat.

Rubio et al. (2007)


Lindsay et al. (2006)

T. Aymerich et al. / Meat Science 78 (2008) 114129

utes, inactivating the vegetative pathogenic and spoilage


microorganisms (>4 log units). For sterilization the range
is over 600 MPa and combination with high temperature
is needed because some spores are even resistant to pressure over than 1000 MPa when temperature is not higher
than 4575 C (Cheftel, 1995). This strategy is now considered to sterilize foods (Heinz & Knorr, 2001) and it is also
the aim of several patents. Mayer (2000) reported in his
patent that a combined heat treatment (over 70 C) with
high hydrostatic pressure (over 530 MPa) with pauses
between two or more cycles was able to achieve a 12D
for Cl. botulinum. The treatment is less severe than conventional retorting and higher quality, texture and retention of
nutrients is achieved (Master, Krebbers, Van den Berg, &
Bartels, 2004).
Prions (bovine spongiform encephalopathy) are also
highly resistant and a pressure treatment of 7001000
MPa at high temperature 60 C 2 h (Fernandez-Garca
et al., 2004) was needed to reduce the survival rate over
the infected meat product by 47%. Also Cardone, Brown,
Meyer, and Pocchiari (2006) reported a reduction on the
level of infectivity of prions from 103 to 106 mean lethal
doses (LD50) per gram of tissue when using a combined
pressure temperature treatment while no autoclave no
alcali no bleach had been eective.
The Scientic Committee on AESA (Spanish Food
Safety Agency) concluded that the technology may be used
for hygienization procedures more than for sterilization of
the meat and meat products. They considered a treatment
of 400500 MPa to be enough to obtain the FSO (food
safety objective) in RTE-products but suggested that a high
treatment of 700800 MPa would be needed to obtain the
FSO in fresh meat products. A higher temperature during
treatment from 30 to 50 C could be useful to obtain the
FSO. Moreover, the microbial resistance and the role of
bacterial stress must be addressed in order to optimize
the treatment and hold the robustness of the technology
into legislation. Dierent stakeholders must interact to
convince consumers of their convenience with objective
and unbiased data including negative aspects and
limitations.
2.3. Biopreservation and natural antimicrobials
In biopreservation, storage life is extended and safety is
increased by using natural or controlled microora, mainly
lactic acid bacteria (LAB) and/or their antimicrobial products such as lactic acid, bacteriocins and others (Hugas,
1998). LAB has a long history of safe use in foods as natural microora of meat, milk, vegetables and sh products.
They can exert its antagonism through competition for
nutrients and/or production of several antimicrobial substances such as organic acids (lactic and acetic), carbon
dioxide, hydrogen peroxide, diacetyl, ethanol, and bacteriocins. They can be an alternative to chemical additives and
act as extra hurdles for food preservation in meat fermentation, and in MAP refrigeration. They could be included

119

in the meat batter, sprayed onto the surface or added


through active packaging depending on the type of product
to be applied. When they are applied as starter cultures,
adjuncts of fermentation or bioprotective cultures, their
success depends on the ability of the culture to grow and
produce the antibacterial factors on the food under the
technological and physicochemical environment (temperature, pH, ingredients, additives, water activity, etc.). Moreover, in fresh meat they must be able to compete with the
endogenous microora. This approach oers and indirect
way to apply antimicrobials and seems the most accepted
way for consumers and producers in fermented meat products and in vacuum packed meats of short shelf-life where
high number of LAB do not aect sensorial characteristics.
When the bioprotective starter is not competitive or may
aect sensorial properties, antimicrobials may be added
as fermentation liquor or as puried substances. In the latter case dosage is more precise but is limited by regulations
on food additives.
Lactic acid and their salts have been extensively used in
meat industry to increase avour and to extent shelf-life of
the product. Their activity against Cl. botulinum, L. monocytogenes, S. aureus, Salmonella and E. coli O157:H7 have
been reported (Aymerich, Jofre, Garriga, & Hugas, 2005;
Glass et al., 2002; Porto et al., 2002; Shelef & Potluri,
1995). In Europe their use is regulated by the European
directive 95/2/CE (European Parliament & of the Council,
1995). In USA it is a recognized antilisterial agent and its
use is regulated by the Federal Register (Food Safety &
Inspection Service, 2000).
Bacteriocins produced by LAB are antimicrobial peptides generally heat stable, apparently hypoallergenic and
readily degraded by proteolytic enzymes in the human
intestinal tract. Although some bacteriocins have been
tested in food, nisin remains the only commercial one
and the only one regulated as an additive by EC (although
not in meat products). They have a long story of safe
use and documented eectiveness against important
Gram-positive food-borne pathogens and spoilage microorganisms.
In fresh meat, nisin has been sprayed to sanitize the surface of red meat carcasses (Cutter & Siragusa, 1994), to
decontaminate articially contaminated pieces of raw pork
(Murray & Richard, 1997). Combined with 2% of sodium
lactate to control S. aureus NMPR3 and Salmonella Kentucky AT1 in fresh pork sausages (Scannell, Hill, Buckley,
& Arendt, 1997) and combined with 2% of sodium chloride
as antilisterial agent in minced raw bualo meat (Pawar,
Malik, Bhilegaonkar, & Barbuddhe, 2000). Pediocin has
also been described as an antilisterial compound in turkey
slurries when combined with sodium acetate (0.30,5%)
(Schlyter, Glass, Loeelholz, Degnan, & Luchansky,
1993). In minced meat, the bioprotective eect of several
LAB and their bacteriocins such as L. sakei Lb706 and
L. sakei CTC494 have been shown as eective antilisterial
agents (Hugas, Pages, Garriga, & Monfort, 1998; Schillinger, Kaya, & Lucke, 1991).

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T. Aymerich et al. / Meat Science 78 (2008) 114129

Their use as natural biopreservatives to overcome the


postprocessing contamination of meat products (slicing,
packaging, peeling and handling) has been reported. Several bacteriocins and their producers have demonstrated
their antilisterial eect on cooked meat products. Sakacin
K and its producer on cooked ham and frankfurter sausages (Hugas et al., 1998), sakacin P and its producer in
vacuum-packed bologna sausages (Krockel, 1997), enterocins in cooked ham, pate and frankfurter sausages
(Aymerich et al., 2000), nisin in frankfurter sausages and
autoclaved tenderloin pork meat (Fang & Lin, 1994;
Hugas, Garriga, Aymerich, & Monfort, 2002), pediocin
in frankfurter sausages and sliced cooked sausages (Hugas,
Garriga, Aymerich et al., 2002; Mattila, Saris, & Tyopponen, 2003) and leucocins and its producer strain (Leuconostoc carnosum 4010) in pork saveloys (Jacobsen, Budde, &
Koch, 2003).
In fermented sausages, where LAB largely dominates,
their biopreservative eects have also been reported.
When several bacteriocinogenic starter cultures where
tested in two dierent technologies (with and without
nitrite), L. sakei CTC 494 turned to be the most ecient
in the rst, while L. sakei Lb706 and L. curvatus
LTH1174 in the second. Pediocin have been reported as
an extra hurdle in fermented sausages (Foegeding, Thomas, Pilkington, & Klaenhammer, 1992), turkey summer
sausages (Luchansky et al., 1992), chicken summer sausages (Baccus-Taylor, Glass, Luchansky, & Maurer,
1993). In salami, Lahti, Johansson, Honkanen-Buzalski,
Hill, and Nurmi (2001) described the antilisterial eect
of a composed starter culture of S. xylosus DD-34 and
the bacteriocinogenic strains Pediococcus acidilactici PA2 and Lactobacillus bavaricus MI401. Enterocins A and
B (Aymerich et al., 2000), CCM4231 (Laukova, Czikkova,
Laczkova, & Turek, 1999; Laukova, Turek, Marekova, &
Nagy, 2003), enterocins 416K1 (Sabia, de Niederhausern,
Messi, Manicardi, & Bondi, 2003), enterocin AS-48 (Ananou et al., 2005) or Enterococcus faecium RZS C5 (Callewaert, Hugas, & De Vuyst, 2000) Enterococcus
casseliavus IM416K1 (Sabia et al., 2003). Also Gill and
Holley (2000) reported the eect of lysozyme when combined with nisin and EDTA, as an eective agent to con-

trol growth of spoilage and safety bacteria in cured meat


products.
In general, antimicrobials provide an excellent opportunity to incorporate into a combined preservation system.
Synergistic eects with HHP have been reported with antimicrobials, low pH, carbon dioxide, organic acids and temperature (Table 4). The eect of lactate, low temperature
storage and HHP treatment on the inactivation of L. monocytogenes is shown in Fig. 3. Also the eectiveness of
selected starter cultures and high hydrostatic pressure
(400 MPa) after ripening was evaluated by Garriga et al.
(2005). Starter cultures were able to control the growth
of L. monocytogenes, Enterobacteriaceae, Enterococcus
and the biogenic amine content. Salmonella spp. counts
decreased signicantly during ripening independently of
the starter culture but the HHP was necessary to ensure
absence of Salmonella in nal products.
There are already a few cultures in the market introduced as starter or bioprotective culture with the aim of
contributing to microbiological safety. Bactoferm F-Lc
from Christian Hansen (Hoershom, Denmark) has been
patented as an antilisterial culture in fermented sausages.
It is a mixed culture of Pd. acidilactici and L. curvatus producing pediocin and sakacin A, respectively. They also
oer other bioprotective cultures for vacuum packed and
MAP meat products containing L. sakei (B-2) and Lc. carnosum 4010 (B-SF-43). Danisco (Copenhaguen. Denmark)
has a combined culture composed of Lactobacillus plantarum and S. carnosus as an antilisterial culture in sliceable
or spreadable sausages and for cooked ham (ALCMix1)
and two more cultures (COX1 and XPA1) for minced meat
and raw sausages either for boiling or frying.
ALTA 2351 and Fargo 23 from Quest International
(B.V., The Netherlands) are natural food ingredients produced through a fermentation process of a bacteriocinogenic Pd. acidilactici strain with antilisterial activity. The
products are approved in the United States and have been
introduced in the market as a shelf-life extender in a great
variety of meat products such as raw sausages, frankfurters, hamburgers and MAP cooked ham. Today nisin is
the only bacteriocin commercially available and accepted
in the positive list of food additives (E234) (European

Table 4
Combined preservation treatments including antimicrobials agents and HHP in meat products
Antimicrobials

Process

Comments

Reference

Nisin

HHP at 350 MPa

Shelf-life of mechanically recovered poultry meat was extended during


30 days at 2 C

Yuste et al. (1998)

Sakacin
Enterocins A and B
Pediocin

HHP at 400 MPa

L. monocytogenes in meat homogenates was kept <102 (CFU/g) for 61


days at 4 C.

Garriga, Aymerich, Costa et al.


(2002)

Pediocin
(ALTA 2351)
Nisin
Potassium lactate

Irradiation
2.3 kGy
HHP at 400 MPa
HHP at 400 MPa

Inhibition of L. monocytogenes in frankfurters during 12 weeks at 4 C


or 10 C
Absence of Salmonella achieved in 50% of the samples
Inhibition of L. monocytogenes in sliced cooked ham during 84 days at
6 C

Chen et al. (2004)


Aymerich et al. (2005)
Aymerich et al. (2005)

T. Aymerich et al. / Meat Science 78 (2008) 114129

121

10
9
8

Log CFU/g

7
6

C6

C1

L6
L1

C6 HHP

C1 HHP

L6 HHP
L1 HHP

0
0

20

40

60

80

Days

Fig. 3. Antilisterial eect of high hydrostatic pressure and lactate salts on spiked sliced cooked ham stored at two dierent refrigeration temperatures 6
and 1 C: Control samples (C6 & C1); samples with lactate (L6 & L1); samples treated with HHP (C6 HHP & C1 HHP) samples with lactate and HHP (L6
HHP & L1 HHP).

Parliament & of the Council, 1995), although its use in


meat products is not regulated. Danisco (formerly Applin
and Barret) and Christian Hansen produces Nisaplin
and Chrisin, respectively, they are both produced from
a fermentation process done by selected strains of Lactococcus lactis subspecies lactis and have the same percentage
of active compound, 2.5%. The use of pediocin PA-1 is patented by Marugg, Ledeboer, Vandenbergh, and Henderson
(1991, EP0493779A1) and enterocin A has a spanish patent
developed by Hugas, Garriga, Monfort, and Ylla (1991, ES
2 068 157). LAB are recognized as safe on the experience of
safe use for USA Food and Drug Administration (FDA)
and the European Commission proposed the term qualied
presumption of safety (QPS) for microorganisms with a
history of safe use (European Commission, 2003b; European Food Safety Authority, 2005).
2.4. Active packaging
In the last decade new packaging systems have contributed to extend the shelf-life of products. At rst MAP,
dened as the enclosure of food in gas barrier material
where the gaseous environment has been changed, was
used. The optimal atmosphere depends on parameters such
as pH, water activity, fat content and type of fat. Although
it must be considered that high concentrations of CO2
could cause collapse of the packaging and increase the loss
dripping due to its solubilization in water and fat, especially in foods with high amount of unsaturated fat (Devlieghere, Debevere, & Van Impe, 1998).
Active packaging is an innovative concept that could be
dened as a packaging system where the pack, the product
and the environment interacts and change the condition of
packed food, extending the shelf life and improving the
food safety or the sensorial properties of the product thus
preserving its quality (European Commission, 2004; Suppakul, Miltz, Sonneveld, & Bigger, 2003; Vermeiren, Dev-

lieghere, & Debevere, 2002). In this system the microbial


substance would gradually migrate from the pack (container) to the food through diusion and partitioning or
release through evaporation in the headspace during storage and distribution, thus being able to reduce the postprocessing contaminations in the surface of the ready-toeat products (Han, 2005). Adhesion on packaging support
and the release (desorption) being critical for eciency.
Moreover, the concentration of the antimicrobial in food
could be reduced when compared to spraying, immersion
or direct addition to the initial meat mixture and interaction/inhibition with food constituents could be avoided
(Coma, 2006). Principal active packaging systems include
oxygen scavengers (absorb oxygen), control of CO2 or ethylene concentration and generation, ethanol and antioxidants releasers, moisture absorption or desiccants and
antimicrobial systems to control the growth of several
microorganisms (Gennadios, Hanna, & Kurth, 1997; Vermeiren, Devlieghere, Van Beest, de Kruijf, & Debevere,
1999). Some of them are commercially available, as shown
in Table 5. The most applied active packaging systems are
oxygen scavengers and/or CO2 generators which are used
to control oxidation of foods and with moisture removers
to prevent spoilage by aerobic bacteria and molds. Active
packaging with a wide spectra of antimicrobials such as
chlorine dioxide, silver substituted zeolite, triclosan
(2,4,4 0 -trichloro-2 0 -hydroxydiphenyl-ether) are also available (Quintavalla & Vicini, 2002). GRAS macromolecules
such as chitosan with lm-forming properties have also
exhibited natural antimicrobial properties against fungi,
yeasts and bacteria (Coma et al., 2002; Ouattara, Simard,
Piette, Begin, & Holley, 2000).
One of the most promising elds is the incorporation of
antimicrobials such as bacteriocins and plants extracts to
the active packaging and their association to biodegradable
packaging such as alginate, zein (natural) or synthetic polyvinil alcohol (PVA) in order to reduce wastes and being

122

T. Aymerich et al. / Meat Science 78 (2008) 114129

Table 5
Active packaging systems and their biological eects
Type of active packaging

Enterprise

Biological eect

Oxygen scavenger and CO2 generators

Ageless-Mitsubishi, Japan
Standa Industry, France
Multisorb Tech., USA
Bioka Ltd., Finland
SouthCorp., Australia

Aerobic spoilage

Chlorine dioxide

Bernard Technologies, USA

Bacteria, fungi, spores and viruses

Silver substituted zeolite

Monroe Engineering Products, USA


Japan

Bacteria, moulds and yeasts

Triclosan
Chitosan

Microban, USA

Bacteriocins (pediocin)

Viskase Co. (patent)

Bacteria, moulds and yeasts


Bacteria (Gram-positive more than
Gram-negatives), moulds and yeasts
Related bacterial species

environmental friendly. Skandamis and Nychas (2002) and


Oussalah, Caillet, Salmieri, Saucier, and Lacroix (2006)
reported the antimicrobial eect of essential oils, although
avour modications are limiting their use in meat products. Some organic acids and theirs salts together with bacteriocins from LAB, mainly nisin, have been applied to
active packaging of meat products with or without biodegradable, edible lms (Table 6). Application of bacteriocins
in active packaging could be an alternative to increase the
eciency of these natural antimicrobials which activity
could be reduced by interaction with the food matrixes.
Four basic categories of antimicrobial lms could be
dened (Cooksey, 2001):
1. Incorporation of the antimicrobial substances into a
sachet connected to the package from which the bioactive substance is released during further storage.
2. Direct incorporation of the antimicrobial into the packaging lm. When applied in a hot extrusion material,
thermoresistant and shearing resistant of the antimicrobial must be considered.

3. Coating of the packaging with a material that acts as a


carrier for the additive. The substance will not be submitted to high temperature or shearing forces, moreover
it could be applied as the later step.
4. Antimicrobial macromolecules with lm forming
properties.
3. Thermal alternative technologies
3.1. High frequency heating
High frequency energy includes microwave and radiofrequency energy and belongs to the non-ionising radiations. Microwaves and radiofrequency have been used for
cooking, drying, blanching, tempering, pasteurising and
thawing (Decareau, 1985). The authorized frequencies
(Institute of Food Technologists, 2000) are included in
the ISM (Industrial, Science and Medicine) bands where
we have 13.56, 27.12 and 40.68 MHz for the radiofrequency range and 433, 915, 2450 and 5800 MHz for the
microwave range.

Table 6
Natural antimicrobials and their use in active packaging
Target

Product

Antimicrobial

LOG reduction
(CFU/g)

Reference

L. monocytogenes

Beef

Alginate coating, with organic acids

1.80 (7 days)

Brochotrix
thermosphacta
L. monocytogenes
Serratia liquefaciens

Beef

Nisin in meat binding, system (Fibrimex)

4.8 (7 days)

Bee steak
Cooked ham

Nisin impregnated, packaged


Chitosan, acetic and lauric acid

3 (21 days)
4.13 log CFU/cm2
(21 days)

Siragusa and Dickson


(1992)
Cutter and Siragusa
(1998)
Schobitz et al. (1999)
Ouattara et al. (2000)

L. innocua
S. aureus

Pork ham

Nisin and Lacticin 3147, in cellulose packaging

2 and 2.8,
respectively

Scannell et al. (2000)

L. monocytogenes

Hamburgers

Up to 1 (1 day)

Mauriello et al. (2004)

L. monocytogenes

Model turkey
frankfurters

Bacteriocin 32Y (Lactobacillus curvatus), on


industrial lm
Nisin and sodium diacetate

Up to 6 (28 days)

Lungu and Johnson


(2005)

T. Aymerich et al. / Meat Science 78 (2008) 114129

There are a great variety of designs for microwave ovens


but all of them share the same principles with a power
source called magnetron and a waveguide to bring the radiation to a cavity where the product is located. A magnetron
has a power between 300 and 3000 W and for industrial
equipment various magnetrons are used to increase the
global power. Most of the ovens have reecting cavity walls
and produce an innity of modes which produce a multimode cavity. A mono-mode or single-mode cavity where
only one mode of propagation is permitted is a more ecient microwave system. The system has a better energy
eciency than the multimode one but the cavity and
waveguides have to be designed geometrically around the
product to be processed. A radiofrequency oven is an
equipment with a generator coupled with a pair of electrodes, called the RF applicator. For industrial equipment
there are two dierent applicators on the market, the rst
called conventional RF equipment where the electrodes
and generator are closely connected and the 50 X RF
equipment where the electrodes and the generator are connected with a high power coaxial cable and controlled by a
matching box. The two systems have advantages and disadvantages and the use of one or the other will depend
of the applications.
The inactivation of microorganism with high frequency
heating is produced by heat and the alternative non-thermal eect of microwave has not been conrmed yet (Institute of Food Technologists, 2000). Several works have been
done to understand the role of dierent parameters during
high frequency heating, such as geometry and composition,
dielectric properties and thermal properties of food product (Ryynamen & Ohlsson, 1996; Wappling-Raaholt &
Ohlsson, 2005). Meat products are complex food systems,
mainly due to the presence of fat and proteins and a variable number of additives. Moisture and salt content are
considered to be key factors in accounting for the dielectric
properties of foods. However, in meat products, other food
components with low dielectric values should not be
neglected due to their sudden temperature rise under
microwave heating. Studies have shown that increase in
fat content results in decrease in dielectric constant and loss

123

factor (Gunasekaran, Mallikarjunan, Eifert, & Summer,


2005). However, several recent experiments (Jeong et al.,
2006; Picouet, Fernandez, Serra, Sunol, & Arnau, 2007)
have shown that fat accelerates the microwave heating rate
and increases the maximum temperature achieved.
High frequency heating, especially in the microwave
bands, can deliver a high temperature in a very short time
resulting in nutritional and sensorial advantages (Orsat &
Raghavan, 2005) over a more traditional technology like
the autoclave one. Moreover, as summarised in Table 7,
the inactivation eect of high frequency has been demonstrated. Paterson, Cranston, and Loh (1995) obtained a
102 CFU/cm2 reductions in bacterial numbers with a
microwave treatment of 2450 MHz. Houben, Schoenmakers, van Putten, van Roon, and Krol (1991) have described
the on-line pasteurization of sausages in a radiofrequency
tunnel of 27.12 MHz frequency with a power between 10
and 25 kW and speed of 120 kg/h. The temperature rose
from 15 to 80 C in the centre of the sausage in 2 min.
On foie gras products, an acceptable pasteurization could
be obtained with a gain of time of 50% and better organoleptic qualities with microwave treatment in comparison
with traditional one (Massoubre, 2003). Additionally, Yilmaz, Arici, and Gumus (2005) have recently compared the
eect of dierent cooking processes (microwave and conventional oven) on meat balls inoculated with E. coli
O157:H7 and S. aureus and higher inactivation rates have
been observed (see Fig. 4). These facts together with the
possibility of oering continuous systems are seen as
advantages in the food processing industry although there
are still non-uniformity problems which must be solved.
Microwave heating and also radiofrequency heating tends
to create hot and cold spots that would depend on the
understanding of parameters such as geometry, composition, dielectric properties and packaging. A way to control
the hot and cold spots generation and therefore accomplish
with the concept of quick ecient decontamination method
(Lacroix, Orsat, Nattress, & Raghavam, 2000), is the use of
vapour inserted in the oven cavity to distribute the heat
and packaging with valves. These designs require well
trained sta and a good maintenance and must be done

Table 7
Eciency of the high frequency treatment on the decontamination of dierent meat products
Target

Product

log reduction (CFU/g)

Process

Reference

Enterococcus
Streptococcus

Vacuum package ham

>4.0

27.12 MHz; 600 W; 600 s

Orsat et al. (2004)

Salmonella
Enteritidis

Fresh chicken thighs

6.4

2450 MHz; 800 Wa; 95 s

Pucciarelli and Benassi (2005)

E. coli O157:H7

Chicken portions

6.0

2450 MHz; 650 Wa; 35 s

Apostolou et al. (2005)

Total ora
E. coli O157:H7
S. aureus

Meat balls

2
>4
>3.5

2450 MHz; 800 W ; 300 s

Yilmaz et al. (2005)

L. monocytogenes

Packaged beef frankfurters

0.94 log(CFU/pk)/min

2450 MHz; 550 W; 360 s

Huang and Sites (2007)

Note: The power indicated correspond to the maximum power of the oven.

124

T. Aymerich et al. / Meat Science 78 (2008) 114129


7
Total bacteria
E. coli O157:H7
S. aureus

Log cfu/g

5
4
3
2
1
0
Control

Conventional Oven

Microwave

Fig. 4. Eect of dierent cooking methods on meat ball inoculated with


E. coli O157:H7 and S. aureus. Microwave process was 5 min treatment at
max power (800 W) with a 2450 MHz oven. The conventional process was
done with an oven at 160 C during 6 min. ND for none detected. Data
extracted from Yilmaz et al. (2005).

in collaboration with microwave and radiofrequency manufacturers and food technical centres with expertise in the
subject.
3.2. Ohmic heating
Ohmic heating process uses the resistance of liquid or
solid products to convert the electric energy into heat (Butz
& Tauscher, 2001). The rate of heat is directly proportional
to the intensity of the electric eld and to the electric conductivity of the sample (Ruan, Ye, Chen, & Doona, 2004).
Although, the ohmic heat technology has proved to be a
successful technology to process liquids, the application
to solid meat products has not yet found industrial application (Piette et al., 2004) and it is at the level of applied
research eld.
The main inactivation mechanism in ohmic heating
seems to be the thermal one, although some reports indicates that other process such as a mild electroporation
mechanism may occur (Institute of Food Technologists,
2000; Ruan et al., 2004). There are only few studies reporting the inactivation eect of ohmic heating on meat based
product. (Piette et al., 2004) reported the inactivation of
Enterococcus faecalis in bologna sausages processed in an
enclosed experimental cooking unit. With this batch system
they were able to have a reduction of 9.06 log10 CFU/g with
a core temperature of 80 C and a total process time of
13.78 min. When the core temperature was reduced to
70 C, the total process time to reach a 9.06 log10 CFU/g
vary from 31.44 to 40.36 min depending on the heating
rate. With a more industrial approach, Zuber (1999) presented the results of the sterilization of a chilli con carne
RTE meal with ohmic heating. The comparison with a conventional heating treatment gave better nutritional and
sensorial qualities while maintaining the safety of the product and reducing the treatment time.

The energy conversion is very ecient as 90% of the


energy can be converted in heat (Ruan et al., 2004). Most
of the disadvantages of the technology are related to the
electrical nature of the food treated. Compounds with poor
conductivity, especially the fat in meat products, do not
generate heat as the same rate than muscle thus creating
a cold spot (Shirsat, Lyng, Brunton, & McKenna, 2004).
In fact, conductivity of the products has to be in the
0.0110 S/min range (Piette et al., 2004). Geometry factors
such as the size of the piece of meat are important factors
and limit the use of the technology. For the pump able system, Zuber (1999) recommends a size of 2 cm. Also other
composition parameters such as the acidity may aect the
best working conditions of the electrodes and reduce the
eciency of the system. Therefore product composition
has to be adapted to the technology Zuber (1999).
3.3. Steam pasteurization
Steam pasteurization process consists in exposing meat
carcasses and meat product to water steam at 8297 C
inside chamber at atmospheric pressure during 612 s.
Normally, the treatment includes the water removal, the
steam pasteurization and a rapid chilling. In some equipment the steam can be combined with pressure to enhance
the eciency of the treatment. The Industrial process was
developed in the US and the steam-pasteurization treatment of carcasses was approved by the FDA in 1995 for
the whole carcasses and parts of carcasses that are to be
further processed.
The eciency of the treatment was exposed in a series of
articles; Nutsch et al. (1998) reported a reduction of
1.0 log CFU/cm2 of the total viable count after a treatment
of 6.5 s at 82.2 C on beef carcasses. Retzla et al. (2004)
had a signicant reduction (>1.0 log CFU/cm2) of E. coli
O157:H7, Salmonella Typhimurium, and Listeria innocua
in beef carcass with a 93.3 C steam treatment during more
than 6 s. Recently, Trivedi, Reynolds, and Chen (2007)
show a reduction of 4.38 log CFU/cm2 on pork skin inoculated by Listeria monocytogenes, using commercial steam
cleaner during 30 s.
On meat products and meat pieces, laboratory apparatus were used and results have been only reported at
research level. Avens et al. (2002) present a reduction of
1.04 log CFU/cm2 of aerobic microbes in chicken carcass
skin with a steam system at 96.7 C during 12 s. McCann,
Sheridan, McDowell, and Blair (2006) show a reduction of
2.4 log CFU/cm2 and 1.5 log CFU/cm2 for, respectively,
E. coli O157:H7 and Salmonella Typhimurium in pork
piece for a steam treatment of 83 C during 15 s.
The technology has the advantage to provide a continuous and cheap solution to decontaminate small and large
pieces of meat product in a very short time. Although for
as noted McCann et al. (2006) and others a prolonged
treatment superior to 10 s give a cooked appearances to
the sample. In carcasses this limiting factor can be overcome leaving the skin. Another disadvantage of the tech-

T. Aymerich et al. / Meat Science 78 (2008) 114129

nology is the homogeneity of the temperature of the steam


has to be carefully checked with a continuous monitoring
system to ensure that the entire surface, especially the neck,
is correctly treated (Nutsch et al., 1998).
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