Atmosfera Modificada Artigo

Chapter IV
Microbiological Safety
of Controlled and
Modified Atmosphere
Packaging of Fresh and
Fresh-Cut Produce
J.N. Farber, L.J. Harris, M.E. Parish, L.R. Beuchat, T.V. Suslow, J.R. Gorney, E.H. Garrett, F.F. Busta
Scope
This chapter addresses the use of modified atmosphere packaging and controlled atmosphere packaging for the preservation of
fresh produce. There have been great technological advances in
this area of preservation, particularly as it refers to improving the
quality and shelf-stability of highly perishable food products, such
as produce. However, when using these technologies, careful attention must be paid to the effect on the survival and growth of
pathogenic organisms. This chapter focuses on food safety aspects of packaging technologies that are either commercially
available or under investigation.
1. Introduction
Over the past 20 years, there has been an enormous increase in
the demand for fresh fruit and vegetable products that has required
the industry to develop new and improved methods for maintaining food quality and extending shelf life (see Chapter I). Due to the
complexities involved with produce, that is, varying respiration
rates which are product and temperature dependent, different optimal storage temperatures for each commodity, water absorption,
by-products, and so on, many considerations are involved in
choosing an acceptable packaging technology. One of the areas of
research that has shown promise, and had success, is that of modified atmosphere packaging (MAP). This technique involves either
actively or passively controlling or modifying the atmosphere surrounding the product within a package made of various types and/
or combinations of films. In North America, one of the first applications of this technology for fresh-cut produce was introduced by
McDonalds (Brody 1995), which used MAP of lettuce in bulksized packages to distribute the product to retail outlets.
The major factors responsible for extending the shelf life of fruits
and vegetables include: careful harvesting so as not to injure the
product, harvesting at optimal horticultural maturity for intended
use, and good sanitation (Moleyar and Narasimham 1994; Lee
and others 1996). When these are practiced, the implementation
of optimum storage conditions through modified atmospheres
can be quite effective at maximizing the shelf life and quality of
the product.
A modified atmosphere can be defined as one that is created by
altering the normal composition of air (78% nitrogen, 21% oxygen, 0.03% carbon dioxide and traces of noble gases) to provide
an optimum atmosphere for increasing the storage length and
quality of food/produce (Moleyar and Narasimham 1994; Phillips
1996). This can be achieved by using controlled atmosphere storage (CAS) and/or active or passive modified atmosphere packaging (MAP). Under controlled atmospheric conditions, the atmosphere is modified from that of the ambient atmosphere, and
142
these conditions are maintained throughout storage. Examples of

this type of storage and the commercial systems available are listed in Table IV-1. MAP uses the same principles as CAS; however,
it is used on smaller quantities of produce and the atmosphere is
only initially modified. Active modification occurs by the displacement of gases in the package, which are then replaced by a
desired mixture of gases, while passive modification occurs when
the product is packaged using a selected film type, and a desired atmosphere develops naturally as a consequence of the products
respiration and the diffusion of gases through the film (Moleyar and
Narasimham 1994; Zagory 1995; Lee and others 1996). The numerous film types used in MAP are listed in Table IV-2, and some
commercially available MAP systems are listed in Table IV-3.
Oxygen, CO2, and N2, are most often used in MAP/CAS (Parry
1993; Phillips 1996). Other gases such as nitrous and nitric oxides,
sulphur dioxide, ethylene, chlorine (Phillips 1996), as well as
ozone and propylene oxide (Parry 1993) have been suggested and
investigated experimentally. However, due to safety, regulatory and
cost considerations, they have not been applied commercially.
These gases are combined in three ways for use in modified atmospheres: inert blanketing using N2, semi-reactive blanketing using
CO2/N2 or O2/CO2/N2 or fully reactive blanketing using CO2 or
CO2/O2 (Parry 1993; Moleyar and Narasimham 1994).
Normally, the concentration of O2 in a pack is kept very low (15%) to reduce the respiration rate of fruits and vegetables (Lee and
others 1995). Reducing the rate of respiration by limiting O2 prolongs the shelf life of fruits and vegetables by delaying the oxidative breakdown of the complex substrates which make up the
product. Also, O2 concentrations below 8% reduce the production of ethylene, a key component of the ripening and maturation
process. However, at extremely low O2 levels (that is, <1%), anaerobic respiration can occur, resulting in tissue destruction and the
production of substances that contribute to off-flavors and offodors (Lee and others 1995; Zagory 1995), as well as the potential for growth of foodborne pathogens such as Clostridium botulinum (Austin and others 1998). Therefore, the recommended percentage of O2 in a modified atmosphere for fruits and vegetables
for both safety and quality falls between 1 and 5% (Table IV-4).
However, it is recognized that the oxygen level will realistically
reach levels below 1% in MAP produce. It is generally believed
that with the use of permeable films, spoilage will occur before
toxin production is an issue; MAP of produce, however, should
always incorporate packaging materials that will not lead to an anoxic package environment when the product is stored at the intended temperature. This recommendation should be qualified,
however, by saying that all films are permeable to oxygen to some
degree; the difference pertains to the rate of gas transfer through
the film, with some films allowing greater transfer rates than oth-
COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETYVol. 2 (Supplement), 2003
Chapter IV: Microbiological Safety of Controlled and Modified Atmosphere Packaging . . .

ers. Moreover, the elimination or significant inhibition of spoilage
organisms should not be practiced, as their interaction with
pathogens may play an integral role in product safety. A number
of packers of fresh prepared green vegetables in the United Kingdom have been experimenting with O2 mixtures between 70 and
100% (Day 1996). The treatment, referred to as oxygen shock or
gas shock, has been found to be very effective in inhibiting enzymatic discoloration, preventing anaerobic fermentation reactions, and inhibiting aerobic and anaerobic microbial growth.
High levels of O2 can inhibit the growth of both anaerobic and
aerobic microorganisms since the optimal O 2 level for growth
(21% for aerobes, 0-2% for anaerobes) is surpassed. However,
there have also been reports of high O2 (that is, 80-90%) stimulating the growth of foodborne pathogens such as Escherichia coli
and Listeria monocytogenes (Amanatidou and others 1999). Recent studies by Kader and Ben-Yehoshua (2000) and Wszelaki
and Mitcham (2000) examining the use of superatmospheric O 2
levels to control microorganisms on produce, have found that
only O2 atmospheres close to 100 kPa or lower pressures (40 kPa
9). in combination with CO2 (15 kPa), are truly effective. These requirements may be difficult to achieve in industry since working
with such high O2 levels can be hazardous due to flammability issues. As with most MAP gases, superatmospheric O 2 has varied
effects depending on the commodity, and further research is required in this area to elucidate the utility of this technique in the
fresh-cut produce industry. A high O2 MAP group has been
formed in the United Kingdom and includes a number of industry
groups, notably Marks and Spencer plc, one of the first retail
chains to distribute MAP foods. More recently, the high O2 MAP
club has provided a base for the new Novel Gases MAP Club
in the United Kingdom, a group that will investigate the use of
novel high 9). argon and nitrous oxide MAP for extending shelf
life and quality of fresh-cut produce. Their main focus is research
into the commercial application of this process.
Nitrogen has three uses in MAP: displacement of O2 to delay
oxidation, retardation of the growth of aerobic spoilage organisms
and action as a filler to maintain package conformity (Parry 1993).
Of the three major gases used in MAP, CO2 is the only one that
has significant and direct antimicrobial activity. A number of theories have been suggested to explain this antimicrobial effect. In
general, CO2 in MAP results in an increased lag phase and generation time during the logarithmic phase of growth of the organisms involved (Phillips 1996), with inhibition being concentration
and temperature dependent. Theories to explain the antimicrobial
action of CO2 have been summarized by Farber (1991):
alteration of cell membrane function including effects on nutrient uptake and absorption;
direct inhibition of enzymes or decreases in the rate of enzyme reactions;
penetration of bacterial membranes leading to intracellular
pH changes;
direct changes to the physicochemical properties of proteins.
The inhibitory action of CO2 has differential effects on microorganisms. Thus, while aerobic bacteria such as the pseudomonads
are inhibited by moderate to high levels of CO2 (10-20%), microorganisms such as lactic acid bacteria can be stimulated by CO2
(Carlin and others 1989; Amanatidou and others 1999). Furthermore, pathogens such as Clostridium perfringens, C. botulinum
and L. monocytogenes are minimally affected by CO2 levels below 50%, and there is concern that by inhibiting spoilage microorganisms, a food product may appear edible while containing
high numbers of pathogens that may have multiplied due to a
lack of indigenous competition (Farber 1991; Zagory 1995; Phillips 1996). More research needs to be done on the interactions of
the background microflora with foodborne pathogens in various
Table IV-1Commercially available controlled atmosphere

systems
Oxygen Control Systems

System
Description
External gas generator
Oxygen is removed from incoming air by

external gas generators which operate on
the open-flame or catalytic burner principles. Fuel as well as CO2 scrubbers are
required; however, the system operation is
very flexible and O2 is rapidly removed.
Liquid nitrogen
The controlled atmosphere is maintained by
atmospheric generators flushing with sprayed liquid nitrogen placed
in front of the evaporator blowers. Excess
CO2 is absorbed by lime bags; a sensor
detects rising O2 levels and corrects them
by spraying more liquid nitrogen.
Gas separator systems Pressure-swing adsorption (PSA) system
The absorption of O2 is mediated by a
filtering system where it is contained in a
membrane; N2 rich gas is exported, and the
bound O2 is flushed by depressurization of
the vessel.
Hollow Fibre Membrane (HFM)
systemCompressed air is heated and
forced through hollow fibers made of
semipermeable membranes; the CO2 and
O2 are selectively removed by the membrane and the N2 continues into the storage
space.
Hypobaric storage
This form of low pressure storage is
mediated by a vacuum pump which
evacuates the container until the desired
pressure is reached. All gas levels are
reduced and ethylene diffusion from the
product is enhanced. Moisture loss is also
reduced. Recommended for the curing of
onions.
Carbon Dioxide Control Systems
These systems are based on scrubbing
action where one of the following 5 reagents
is used: caustic soda, water, hydrated lime,
activated charcoal, and molecular sieves.
All involve the removal of CO2.
Ethylene Control Systems
Ethylene can be removed by means of a
scrubber-heated catalyst system where
ethylene is oxidized to yield CO2 and water
vapor, which is then removed from the
room, or by means of an absorbent bead
scrubber where ethylene is bound to
aluminum silicate spheres mixed with
potassium permanganate. In the latter, as
bead saturation occurs, they turn from
purple (KMnO4) to brown.
(Raghavan and others 1996).
modified atmospheres used for produce, as well as on the effects

of different gaseous environments on the survival and growth of
bacterial foodborne pathogens on whole and fresh-cut produce.
The optimal MAP conditions for produce quality and respiration
for a number of fruits and vegetables are listed in Table IV-4.
1.1. Types of CAS
There are a number of commercially available systems for CAS

(Table IV-1). There are advantages and disadvantages to each, and
generally the active control systems are most costly due to the
need for constant maintenance of gas levels. Since this type of
storage is used for large quantities of product, and is not a type of
Vol. 2 (Supplement), 2003COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY
143
IFT/FDA Report on Task Order 3

Table IV-2Polymers, film types and permeability available for packaging of MAP produce
Permeability(cm3/m2.d.atm for 25 mu film at 25 C)

Film
Oxygen
Nitrogen
Carbon dioxide
3-5
9-15
7800
2600
3700
2000
10-20
150-350
500-30000
12500
5000
800-1500
8-25
40
>15,0004
>15,0004
2800
650
680
400
8-13
60-150
300-10000
4900
800
600-1200
2-2.6
14
20-30
42000
7600
10000
8000
35-50
450-1000
1500-46000
50000
18000
7000-25000
50-150
150-190
16-18
18
7-10
10-12
6-7
4-5
30-40
15-40
40-60
100-125
400-600
1.5-5.0
84-3100
Variable
O2 permeability
(mL.mm/m 2 .d.atm)
CO2 permeability
(mL.mm/m 2 .d.atm)
Relative Humidity
57.5
91.4
190/250
77
153
133
83
46.6
4
<3
<3
78.8
0.362
0.892
8.32
0.552
2.102
1553
4750/7100
462
1705
1282
154
180
27
15
13
2.672
5.252
26.12
87
93
91/94.5
77
94.5
91
48
52
42
56
56
100
0.1163
0.4073
0.000653
0.000423
Ethylene-vinyl alcohol (EVOH)

Polyvinylidene chloride coated (PVdC)
Polyethylene, LD
Polyethylene, HD
Polypropylene cast
Polypropylene, oriented
Polypropylene, oriented, PvdC coated
Rigid PVC
Plasticized PVC
Ethylene vinyl acetate (EVA)
Polystyrene, oriented
Polyurethane (polyester)
PvdC-PVC copolymer (Saran)
Polyamide (Nylon-6)
Microperforated (MP)
Microporous, (MPOR)
Edible Films
Water vapor
transmission, g/m2/day/atm
(38 C and 90%
relative humidity)
Pectin
Chitosan
Wheat (gluten)
Na caseinate
Gluten-DATEM
Gluten-beeswax
Na casenate/Myvacet
MC/MPMC/fatty acids
MC and beeswax
Gluten-DATEM and beeswax
Gluten-Beeswax and beeswax
Methylcellulose-palmitic acid
Zein
Cozeen
Polyethylene
Polypropylene
Sucrose polyester
Smart Films
O2 scavengers with O2 indicators

antibody based detection systems for detection of microbial pathogens
Antimicrobial films
(i) Edible
Chlorinated phenoxy compound with biocide incorporated into the polymer layer (that is, nisin, lysozyme)
Chlorine dioxide with biocide incorporated into polymer layer$Edible films with sorbic acid, sodium benzoate, benzoic acid and potassium
sorbate
Pine based volatiles added to edible film$Horseradish extract added to edible film
(ii) Non-edible films/products
Propyl paraben dispersed in a polymer emulsion (Permax 801 or Carboset)
LDPE with Imazalil
LDPE with grapefruit seed extract$Gas, as produced by sachets or other materials to produce sodium metabisulfite to obtain the production
of sulfite
(Day 1993; Greengrass 1993; Guilbert and others 1996; Phillips 1996; Chung and Yam 1999; Park 1999; Han 2000)
*Information not available.
1Dependent on moisture (Day 1993).
2Unit of permeability is in fl .m/m 2.s. Pa; f is abbreviation for femto (10-15).
3Unit of permeability is ng. m/m2. s.Pa; n is the abbreviation for nano (10-9).
4Oxygen transmission rate, dependent on film and degree of microperforation or microporosity (Day 1993).
HPMC=hydroxypropyl-methylcellulose; MC=methylcellulose; DATEM=diacetylated tartaric ester of monoglycerides; AM=acetylated monoglycerides
packaging, it will not be discussed further.

1.2. Types of MAP
MAP is used mainly for wholesale/foodservice use and retail

display. There are many MAP systems currently in use (Table IV-3).
The films used for MAP of fresh-cut produce (Table IV-2) will be
144
discussed briefly.
1.2.1. Bulk packaging. Bulk packaging is similar to CAS, but relies on a passively modified atmosphere (Lee and others 1996).
This type of packaging is mainly used for pallet bags and paperboard containers used in the transportation and storage of commodities. These films can be ecologically advantageous since

Table IV-3Commercially available modified atmosphere packaging systems for small and large quantities of produce
Product 1
Description
Use
Pallet Package System
Pallet box wrapped in heavy gauge polyethylene, with a silicone

membrane window to allow gas exchange regulation and a
calibrated hole for pressure regulation.
For room storage: regulates the atmospheric composition via a
parallel series of rectangular bags of silicone rubber; can be
installed in or out of storage area and maintains a fairly consistent
atmosphere.
System of gas diffusion panels enclosed in an airtight container,
having two separate airflow paths and a control panel, allowing the
potential for automation.
Pallet box bulk unit-wrapped with a barrier plastic film; gases are
injected and the bag-sealed.
Long, narrow box overwrapped with gas permeable film;
contains a sachet containing calcium chloride and activated lime to
absorb CO2.
Consists of a breathable plastic membrane in the liner of the walls
of a corrugated paperboard FreshSpanTM box, which can be
hermetically sealed.
Maptek Fresh is a postharvest biotechnology where specific
features and conditions are applied for each type of product to
stabilize the produce and place it in a state of hibernation.
Curwood provides a variety of films for produce packaging and
can add a variety of features to the package such as antifog,
EZ Peel, Peel-Reseal, Integra Tear and Magic Cut.
This system incorporates the optimal atmosphere by testing, to
choose the exact gas mixture and the best film for each product
considering respiration rate, temperature, packaging film, pack
volume, fill weight and light.
Polypropylene label with calcium carbonate embedded in it.
Apples, pears and other perishables
Marcellin System
Atmolysair System
Tectrol System
(TransFRESH Co.)
Tom-Ah-Toes
(Natural Pak Produce)
FreshSpanTM (Sun
Blush Technologies Inc)
MaptekFreshTM (Sun
Blush Technologies Inc.)
FreshflexTM (Curwood)
MAPAX (AGA, Sweden)
FreshHold
(Hercules Chemical Co.)
Cryovac(W.R. Grace
and Co.)
Propafilm CR and CK
(Imperial Chemical
Industries PLC)
P-Plus films
(Courtaulds Packaging)
T-grade (CVP Systems)
Clysar EHC, EH, ECL,
LLP(DuPont)
Laminated boxes(Georgia
Pacific, Weyerhaeuser and
Tamfresh Ltd.)
Film Convertors
0.75, 1.25, 2.5 mm thick bag made of several layers of

polyethylene related polymers.
Polypropylene-based films.
Various perishables
Cabbage in Canada, other perishables

Strawberries for short term transport
Avocados, tomatoes, mangoes
Fresh-cut asparagus, broccoli,

cauliflower, avocados, berries, stone
fruit
Fresh-cut produce: pineapple, fruit
salad, cut tomatoes, mango, kiwi,
melon, citrus fruits
Produce
Fresh-cut produce, lettuce,

mushrooms, pre-peeled potatoes
Broccoli, asparagus, cauliflower and

cherries
Cut lettuce, broccoli, cauliflower,
spinach, peeled potatoes and other
fresh fruits and vegetables
Fresh-cut lettuce and other
vegetables
Spark perforated films which result in non-uniform perforations

throughout the film to facilitate gas exchange.
Films are coextruded bilayer films in 1.0, 1.25, 1.5 and
1.75 mm thickness.
Biaxially oriented, heat shrinkable polyethylene or polyolefin films.
Brussels sprouts, lettuce, broccoli,

fresh mushrooms, and bean sprouts
Cartons with films laminated within the cardboard or coated on

the inside of the cardboard liner. Reduces moisture loss and
potentiates air flow.
The converters (companies) buy resin or film and adapt it to
attractive specifications. Converters are often more flexible with
respect to specific applications of the requested film.
Strawberries, broccoli, and other

perishables
Variable/product specific
Edible Films1
TAL Pro-Long
(Courtaulds Group)
Nutri-Save
Semperfresh, Nu-Coat Fo,
Ban-seel, Brilloshine,
Snow-White and White
Wash products (Surface
Systems Intl. Ltd.)
Blend of sucrose esters of fatty acids and sodium carboxymethyl

cellulose; depresses internal O2 and is edible.
N, O-carboxymethychitosan edible film.
Sucrose ester based fruit coatings with sodium carboxymethyl
cellulose products manufactured exclusively from food
ingredients available in dip or spray.
Pears
Pears, apples
Most fruits and vegetables, processed
and whole potatoes (Snow-White
and White-Wash)
(continued on next page)

145

Table IV-3Commercially available modified atmosphere packaging systems for small and large quantities of produce
(continued from previous page)
Product 1
Description
PacRite products (American Variety of products, water-based carnauba-shellac emulsions,

Machinery Corp.)
shellac and resin water emulsions, water-based mineral oil fatty
acid emulsions, and so forth.
Fresh-Cote product line
Variety of products including; shellac-based, carnauba-based and
(Agri-Tech Inc.)
oil emulsion edible films.
Vector 7, Apl-Brite 300C, Vector 7 is a shellac-based film with morpholine; the Apl-Brite and
Citrus-Brite 300C
Citrus-Brite are carnuba-based films.
(Solutec Corp.)
Primafresh Wax
Carnauba-based wax emulsion.
(S.C. Johnson)
Shield-Brite products
Shellac, carnauba, natural wax and vegetable oil/wax and xanthan
(Pace Intl. Shield-Brite)
gum products.
Sta-Fresh Products
Natural, synthetic, and modified natural resin products and
(Food Machinery Corp.)
combinations thereof.
Use
Apples, citrus, tomatoes, cucumbers,

green peppers, squash, peaches,
plums, nectarines
Apples, pears, eggplant, tomatoes,
cucumbers, stone fruits
Apples and citrus fruits
Apples, citrus and other firmsurfaced fruit

Citrus, pears, stone fruit
Citrus, apples, stone fruits, pomegranates, tomatoes, pineapple, canta

loupes, and sweet potatoes
Fresh Wax products
Shellac and wood resin, oxidized polyethylene wax, white
Citrus, cantaloupes, pineapples,
(Fresh Mark Corp.)
oil/paraffin wax products.
apples, sweet potatoes, cucumbers,
tomatoes and other vegetables
Brogdex Co. products
Carnauba wax emulsions with or without fungicides, emulsion wax, Apples, melons, bananas, avocado,
high shine wax, water-based emulsion wax, carnauba-based
chayote, papaya, mango, pineapple,
emulsion, vegetable oil, resin-based and concentrated polyethylene citrus, stone fruits.
emulsion wax products.
Currently available for avocado,
FreshSealTM (Planet Polymer A patented coating that slows the ripening process by controlling
Technologies Inc. has
the O2 and CO2 and water vapor flowing in and out of the product. cantaloupe, mangoes and papaya.
licensed CPG Technologies It can be tailored to the individual respiration rates of different fruit
Use on limes, pineapples and
of Agway, Inc. to produce) and vegetable varieties.
bananas is currently under
investigation.
Composite polysaccharide-based coating using cellulose derivatives Sliced apples, carrots, peppers,
Nature-SealTM, AgriCoat
(Mantrose Bradshaw
as film formers.
onions, lettuce, pears, avocados,
Zinsser Group)
sliced bananas
Intelligent Systems
Activated Earth Films
Typically polyethylene bags with powdered clay material made of

powdered aluminum silicates, incorporated into the film matrix.
Possibly reduces ethylene concentration by facilitating its diffusion
out of the bag.
Temperature Responsive
Films increase their gas permeabilities in response to temperature
Films(Landec Labs)
increases as well as increases in respiration. Stabilizes the modified
atmosphere so it remains the same under various temperatures.
CO2 ScavengersFreshLock Sachet type product which is placed directly in the package and
(Mitsubishi Gas Chemical absorbs both carbon dioxide and oxygen.
Co.), Verifrais (Codimer
Tournessi, Gujan-Mestras)
Ethylene absorbents
Sachet type product which is placed directly in the package and
Ethysorb (StayFresh Ltd),
absorbs ethylene. They are composed of a variety of products
Ageless C (Mitsubishi Gas such as aluminum oxide, potassium permanganate, activated
Chemical Company),
carbon, and silicon dioxide.
Freshkeep (Kurarey),
Acepack (nippon Greener),
Peakfresh (Klerk Plastic
Industries, Chantler
Packaging Inc.)
Variable
Specific for each product
Fruits and vegetables, coffee
Fruits and vegetables
Antimicrobial Films
-unsure of commercial availability
(Church 1993; Baldwin 1994; Zagory 1995; Lee and others 1996; Raghavan and others 1996; Smith and Ramaswamy 1996; Padgett and others 1998; Han 2000).
1 Different film types discussed in Table IV-2.
146

Table IV-4Some characteristics and optimum storage conditions of whole fruits and vegetables for MAP
Tolerance
Commodity
Optimum
Respiration Rate
(at 5 C, mg CO2/kg/h)
Maximum
CO2 (%)
Minimum
O 2 (%)
CO 2
(%)
O2
(%)
Recommended
storage temp.
Approximate
storage life
5-10
10-20
10-20
15a
10-20
20-40
2-5
2
5
5
15
15
10
5
5
5
2
10
15
1-2
2
3
2
2
2
5
2
2
2
2
1-3
2-3
3-10
2-5
15-20
12-20
10-12
0-5
15-20
1-3 or 10-15
5-10
3-5
0-10
0-10
5-8
3-5 or 15-17
0-5
5-8
3-5
0-1
5-8
5-10
5-10
15-20
15-20
1-2
2-3
2-5
2-5
5-10
2.5
3-10
1-2
5-10
2-5 or 5-10
3-10
1-2
5-10
5-10
3-7
1-2 or 4-6
5-10
2-5
1-2
2-3
3-5
2-5
3-5
5-10
5-10
0-3
0-5
5-13
12-15
0-5
0-5
3-7
0-5
2-5
0-5
0-5
10-15
0-5
10-15
10-15
10-15
0-5
5-10
10-15
0-5
0-5
0-5
8-13
5-10
0-5
0-5
2-11m
8-10d
15d
6m
>60
40-60
>60
40-60
10-20
10-20
20-40
10-20
>60
4b
10-20
>60
10-20
>60
10-20
10-20
5-10
5-10
2
14
10?
10
5
5
5
5
2
15
10
2
15
2
15
2
2
3
5
2
1
2
2
5
2
3
2
3
2
1
3
3
3
2-3
10-14
5-10
5-10
5-7
3-6
3-4
2-5
5
10-20
0
0
5-15
0
10-20
0
3-5
none
0
2-3
Air
2-3
1-2
1-2
2-3
5
2-5
3
2-4
3-5
1-3
3-21
3-5
air
3-5
3-5
none
1-2
0-5
1-5
5-10
0-5
0-5
0-5
0-5
0-5
8-12
0-5
8-12
0-5
0-5
8-12
0-5
12-20
10-15
4-12
0-5
29d
21d
7-10d
2-3m
2-3m
6-12m
4-5m
2-3m
14-21d
3-4wks
3-4d
2-3wks
2-3wks
2wks
8m
Fruit
Apple
Apricot
Avocado
Banana
Blackberry
Blueberry
Cantaloupe
Cherry (sweet)
Cranberry
Fig
Grape
Grapefruit
Kiwifruit
Lemon
Lime
Mango
Nectarine
Orange
Papaya
Peach
Pear
Persimmon
Pineapple
Pomegranate
Raspberry
Strawberry
Vegetable
Artichoke
Asparagus
Beans, snap
Broccoli
Brussels sprouts
Cabbage
Carrot
Cauliflower
Chili peppers
Corn, sweet
Cucumber
Lettuce (leaf)
Mushrooms
Bell peppers
Spinach
Tomatoes (mature)
Tomatoes (partly ripe)
Potato
Onion
(Adapted from Powrie and Skura 1991; Day 1993; Exama and others 1993; Moleyar and Narasimham 1994; Smith and Ramaswamy 1996).
a At 10 C in air (Day 1993).
b At 10 C in 3% O (Day 1993).
2
some are returnable, and thus reuse is possible in some cases. An

example of this kind of packaging is the Marcellin System (Table
IV-3).
1.2.2. Prepackaging. Following bulk packaging and arrival at
the retail outlet, produce can be prepackaged by the grocer or the
customer using a passive MAP (Smith and Ramaswamy 1996).
Prepackaging in the store usually involves the use of plastic film
packaging such as low density polyethylene (LDPE), polyvinylchloride (PVC) or polypropylene (PP); films which help to minimize moisture loss and maintain produce quality (Lee and others
1996). However, the films used often supply only a narrow range
of gas selectivity and due to its imprecise nature, this type of packaging is only applicable to a few products.
In-store packaging has recently been applied to the new online

grocery shopping and delivery services. A number of online grocery stores, such as www.peapod.com and www.netgrocer.com
in the United States, and www.grocerygateway.com and
www.onlinegrocer.ca/shop/home.asp in Canada, have recently
been established. The most comprehensive of these organizations
will ship everything from fresh fruits and vegetables and staples to
frozen and fresh meat and seafood products. It does not appear
that these services use any special packaging in addition to that
already used in the grocery store. However, it is recommended
that attention be paid to this growing online service, especially in
terms of the potential for cross-contamination in the warehouse
and temperature abuse during storage and/or transportation.
147

Table IV-4bControlled and modified atmosphere storage
recommendations for selected fresh-cut fruits and vegetables
Fresh-cut Vegetables
Product
Beets (Red), Grated,
Cubed or Peeled
Broccoli, florets
Cabbage, Shredded
Cabbage, (Chinese),
Shredded
Carrots, Shredded,
Sticks or Sliced
Leek, Sliced
Lettuce (Butterhead),
Chopped
Lettuce (Green Leaf),
Chopped
Lettuce (Iceberg),
Chopped or Shredded
Lettuce (Red Leaf),
Chopped
Lettuce (Romaine),
Chopped
Mushrooms, Sliced
Onion, Sliced or Diced
Peppers, Diced
Potato, Sliced or
Whole-Peeled
Rutabaga, Sliced
Spinach, Cleaned
Tomato, Sliced
Zucchini, Sliced
Fresh-Cut Fruits
Apple, Sliced
Cantaloupe, Cubed
Honeydew, Cubed
Kiwifruit, Sliced
Orange, Sliced
Peach, Sliced
Pear, Sliced
Persimmon, Sliced
Pomegranate, arils
(seed coating)
Strawberry, Sliced
Atmosphere
Temp.
(C)
O2 (%)
CO2 (%)
Efficacy
0-5
0-5
0-5
5
2-3
5-7.5
5
6-7
15
Moderate
Good
Good
0-5
Moderate
0-5
0-5
2-5
5
15-20
5
Good
Moderate
0-5
1-3
5-10
Moderate
0-5
0.5-3
5-10
Good
0-5
0.5-3
10-15
Good
0-5
0.5-3
5-10
Good
0-5
0-5
0.5-3
3
5-10
10
0-5
0-5
2-5
3
0-5
0-5
0-5
0-5
5
1-3
5
0.8-3
3
0.25-1
6-9
5
8-10
3
Good
Moderate
Moderate
Moderate
Moderate
0-5
0-5
0-5
0-5
0-5
0
0-5
0-5
<1
3-5
2
2-4
14-21
1-2
0.5
2
6-15
10
5-10
7-10
5-12
<10
12
Moderate
Good
Good
Good
Moderate
Poor
Poor
Poor
0-5
0-5
1-2
15-20
5-10
Good
Good
Good
Not
recommended
10-15
Good
5-10
Moderate
Reproduced from Gorny (1997) by permission of J.R. Gorny.
1.3. Films used in MAP
The use of MAP for whole and fresh-cut produce involves careful selection of the film and package type for each specific product and package size (Tables IV-2 and VI-3). Effective MAP of produce requires consideration of the optimal gas concentration,
product respiration rate, gas diffusion through the film, as well as
the optimal storage temperature in order to achieve the most benefit for the product and consumer. In addition, when selecting an
appropriate film, one has to take into account the protection provided, as well as the strength, sealability and clarity, machineability, ability to label, and the gas gradient formed by the closed film
(Zagory 1995).
Recently, the long list of films and commercially available MAP
systems has been augmented with the conception of both smart
148
and edible packaging systems (Guilbert and others 1996; Phillips

1996). Smart or intelligent packaging is being used in the
fresh-cut industry and includes indicators of time and temperature, gas composition, seal leakage, and food safety and quality
(Rooney 2000). Some intelligent systems alter package oxygen
and /or carbon dioxide permeability by sensing and responding
to changes in temperature. Other smart films incorporate chemicals into packets placed in the packaging system, with no contact
with the product; an example would be the use of O2 scavengers
with O2 indicators. Another type of smart film, developed with
food safety in mind, is currently undergoing testing. This novel
system, when incorporated into a packaging film, uses an antibody detection system to detect pathogens, and expresses a positive finding as a symbol on the surface of the package, thereby
alerting food handlers to the presence of pathogens. Although this
technology shows promise, it is still in its infancy and comprehensive assessments have yet to be performed. Several limitations
have been suggested with this technology; for example, it would
not likely be able to detect pathogens at concentrations below
104 CFU/g or cm2 and would not detect pathogens within the
product.
Edible biodegradable coatings are yet another variant of the
smart film technology, where a film is used as a coating and applied directly on the food (Guilbert and others 1996; Francis and
others 1999). Wax has been used in China since the 12th and
13th centuries as an edible coating to retard desiccation of citrus
fruits, and in the last 30 years, edible films and coatings made
from a variety of compounds have been reported. Guilbert and
others (1996) and Baldwin (1994) have extensively reviewed
some of the newer edible films (see Tables IV-3 and VI-5). These
films are gaining popularity due to both environmental pollution
and food safety concerns (Padgett and others 1998). However, a
number of problems have also been associated with edible coatings. For example, modification of the internal gas composition of
the product due to high CO2 and low O2 can cause problems
such as anaerobic fermentation of apples and bananas, rapid
weight loss of tomatoes, elevated levels of core flush for apples,
rapid decay in cucumbers, and so on (Park and others 1994).
Edible films may consist of four basic materials: lipids, resins,
polysaccharides and proteins (Baldwin and others 1995). Plasticizers such as glycerol as well as cross-linking agents, antimicrobials, antioxidants, and texture agents can be added to customize
the film for a specific use (Guilbert and others 1996). Plasticizers
have the specific effect of increasing water vapor permeability.
Therefore, their addition must be considered when calculating the
desired water vapor properties of each specific film, since too
much moisture can create ideal growth conditions for some foodborne pathogens. The most common plasticizer used to cast edible films is foodgrade polyethylene glycol, which is used to reduce film brittleness (Koelsch 1994).
Lipids, or waxes and oils, and resins such as shellac and wood
rosin have been widely used for intact fruits and vegetables in two
distinct forms, laminates and emulsions (Baldwin and others
1995). Lipid-based edible barriers are known for their low water
vapor permeabilities. Koelsch (1994) found that the water vapor
permeability of a cellulose-based emulsion barrier is dependent
on the lipid moiety used; a minimum permeability can be
achieved when stearic acid is used as the lipid. This is due to the
effective barrier formed by stearic acid through an interlocking
network. However, lipid-based edible films also require a support
matrix to reduce brittleness, and have difficulty adhering to the
hydrophilic cut surfaces of fruits and vegetables (Koelsch 1994;
Baldwin and others 1995). Some of the most common compounds used for support matrices are modified celluloses of hydroxypropylmethyl, ethyl and methylcellulose, chitosan and
whey protein isolate (WPI; Koelsch 1994).

In general, polysaccharides such as cellulose, pectin, starch,
carrageenan, and chitosan, can adhere to cut surfaces of produce
and effectively allow gas transfer; however, they are not effective
moisture barriers. Due to their CO2 and O2 permeabilities,
polysaccharide-based films allow the creation of desirable modified atmospheres, an attractive advantage over plastic or shrink
wrap MAP which can be labor intensive, expensive and environmentally harmful (Baldwin and others 1995). A number of cellulose derived coatings are available commercially, most taking advantage of the modified atmosphere effect of the barriers. Pro-long
(Courtaulds Group, London) and Semperfresh (Surface Systems
International, Ltd., Oxfordshire, U.K.) are examples of water-soluble composite coatings comprised of the sodium salt of carboxymethyl cellulose (CMC) and sucrose fatty acid ester emulsifiers (Baldwin and others 1995). Their properties are discussed in
Table IV-6. A newer product called Snow-White, based on sucrose esters of fatty acids, has also been used to combat oxidative
browning in the potato industry. Nature-Seal is a polysaccharidebased surface treatment that uses cellulose derivatives as film
formers, but unlike Semperfresh and Pro-long, does not contain
sucrose fatty acid esters. Nature-Seal is a browning inhibitor that
is applied as a dip or spray and has been shown to delay ripening
of whole fruits and vegetables, and to retard discoloration of
peeled carrots and cut mushrooms.
Finally, proteins such as casein, soy, and zein, can also adhere
to hydrophilic cut produce surfaces and are easily modified to
form films; however, they also allow water diffusion (Baldwin and
others 1995). Unlike lipid-based barriers, protein-based barriers
do not require the addition of a support matrix, since the protein
acts as both the water vapor barrier and structural component of
the film (Koelsch 1994). Park and others (1994) reported the successful application of a corn-zein film to extend the shelf life of tomatoes. Color change, loss of firmness, and weight loss during
storage were delayed, and shelf life was extended by 6 days in
comparison to untreated tomatoes. The corn-zein product used in
the above study was a commercial product that was brushed onto
the tomatoes (Regular Grade F4000, INC Biomedicals, Inc.), and
consisted of 54 g of corn-zein, 14 g of glycerine, and 1 g of citric
acid dissolved in 260 g of ethanol. Park and others (1994) did not
comment on the use of citric acid in the film solution; however,
others have found that edible films composed of zein were more
successful in preventing the rancidity of nuts when citric acid was
added (Guilbert and others 1996).
In order to obtain an edible film that incorporates all the best
qualities of these four basic materials, as well as fulfilling the specific conditions for each fruit or vegetable, manufacturers are now
producing films comprised of different combinations. Some of the
advantages and disadvantages of the four basic edible film barriers, as well as combinations thereof, are listed in Table IV-5.
As with other MAP technologies, edible films can create a very
low O2 environment where anaerobic pathogens such as C. botulinum may thrive; however, antimicrobial compounds can be incorporated into the coating in this scenario (Guilbert and others
1996). Since the antimicrobial or antioxidant can be incorporated
and applied directly to the surface of the product, only small
quantities are required. Not all films are equally amenable to the
addition of antimicrobials. Much of the current work on antimicrobial films is taking place in Europe. Some of the incorporated
antimicrobial compounds include metal ions supported in zeolite, isothiocyanate in cyclodextrin with cobalt ion, chitosan, allyl
isothiocyanate, silver-based fungicide, quaternary ammonium
salt, organic monoglycerides, copper and zinc (Padgett and others
1998), benzoic acid, sodium benzoate, sorbic acid and potassium sorbate and propionic acid (Baldwin and others 1995). Researchers are also currently looking at the use of nisin, a bacteriocin, in coatings to suppress L. monocytogenes, as well as other
bacteriocins for the control of C. botulinum. Successful applications of this technology have been demonstrated using sodium
caseinate/stearic acid to coat peeled carrots and caseinate/acetylated monoglyceride to coat celery sticks (Guilbert and others
1996). Zhuang and others (1996) investigated the ability of a hydroxypropyl methylcellulose coating containing various antimicrobials to inactivate Salmonella Montevideo on the surface and
in the core tissues of tomatoes. Citric or acetic acid (0.2, 0.4%)
did not enhance inactivation; however, 0.4% sorbic acid significantly enhanced the inactivation of S. Montevideo, although the
tomatoes had a chalky and unappealing appearance. A study performed by Padgett and others (1998) did not specifically look at
the application of antimicrobial films to food products; however,
the incorporation and behavior of antimicrobials in edible films
were observed. Padgett and others (1998) examined the inhibitory
effect of both lysozyme and nisin, incorporated directly into corn
zein and soy protein films, against a gram-positive and gram-negative indicator organism. They found that casting, rather than heat
pressing during the processing of films, was more effective at producing an antimicrobial film when using corn and soy films. Also,
the antimicrobial additives affected the film structure as fracture
lines were noted at the microscopic level when lysozyme was incorporated, potentially affecting the film integrity. Following incorporation into the films, both nisin and lysozyme maintained their
antimicrobial capacity against the indicator organisms Lactobacillus plantarum and E. coli, which was augmented by the addition
of a chelating agent such as EDTA (Padgett and others 1998).
In addition to the study performed by Padgett and others
(1998), there have been many studies investigating the migration
of additives such as antimicrobials from coatings into food (Guilbert and others 1996). Sodium benzoate, benzoic acid, propionic
acid, and potassium sorbate are also generally recognized as safe
(GRAS) food additives, and sorbic acid has become a model additive for migration studies. In general, wheat gluten-glycerol films
containing lipid components, resulted in a 50% reduction in the
diffusivity of sorbic acid out of the film. Films composed entirely
of lipids allowed even less diffusion of sorbic acid. Therefore, the
most advantageous use of these films for antimicrobial properties
would be the formation of a monolayer lipid and sorbic acid film,
or a bilayer film composed of a hydrophilic base layer coated
with a thin layer of lipid containing sorbic acid (Guilbert and others 1996). Chen and others (1996) attempted the construction of
an antimicrobial film containing chitosan (water resistant) and methylcellulose (water susceptible), and either sodium benzoate or
potassium sorbate as antimicrobials. Although the film was found
to be inhibitory to fungi as judged by inhibitory zones on agar
media, release of the antimicrobials from the film was too high to
maintain a continuous and effective concentration of the antimicrobial in the film.
Antimicrobial compounds have also been used with traditional
films such as low-density polyethylene (LDPE); for example, the
fungicide Imazalil (IM) and the antimicrobial grapefruit seed extract (GFSE) have recently been used with bell peppers and lettuce, respectively (Miller and others 1984; Han 2000). In the
study using IM, it was noted that the use of IM and IM impregnated film was more effective than either treatment alone at controlling fungal decay; however, IM impregnated film increased the incidence of bacterial soft rot (Miller and others 1984). The action of
this fungicide on potential pathogens is unknown. Lee and others
(1998) investigated the ability of GFSE with LDPE films to inhibit
growth of E. coli, Staphylococcus aureus, molds, yeasts, and lactic
acid bacteria, using the plate disk test. Films containing 1.0%
GFSE in LDPE film inhibited E. coli and S. aureus as demonstrated
by a clear zone; however, molds, yeasts and lactic acid bacteria
were unaffected. After testing the films using the plate disk test,
Lee and others (1998) used the films for packaging of curled let-
149

Table IV-5Properties and characteristics of edible films
Film
Film Preparation
Advantages
Disadvantages
Simple coacervationa
Complex coacervationa
Gelatin or thermal coagulationa
Polysaccharide/Protein
biodegradable and renewable
used to replace short shelf life
plastics
suitable overall mechanical
and optical properties
good for high-moisture foods
Lipids/Polyesters
biodegradable and renewable
good water vapor barrier
properties
Polysaccharide/Protein
highly sensitive to moisture
and has poor water vapor
barrier properties
General Films
Natural biopolymer films: composed of
polysaccharides, polyester proteins,
lipids and derivatives
Lipids/Polyesters
reduction of moisture transport
opaque and relatively inflexible
can be fragile and unstable
Lipid-Based Coatings (Koelsch 1994)

Emulsions
Laminates
non-lipid support matrix required lower water vapor permeability

to reduce brittleness
than laminate barriers
lipid added to an emulsion barrier
when cellulose within support
matrix is dissolved
when mixed (lipid/support matrix),
the barrier is cast using i
mpenetrable glass or metal level
plate
water and ethanol are removed,
and the barrier dried to moisture
content of 2-5%, and then peeled
from plate
molten lipid is either painted,
easier to apply than emulsions
sprayed, or poured to form a
distinct layer on the dry support
matrix
laminate is then dried/cooled,
peeled off and stored until use
requires non-lipid support

matrix
requires non-lipid support

matrix
Protein Barriers (Koelsch 1994; Baldwin and others 1995; Guilbert and others 1996)
Casein, collagen, corn zein, gelatin, soy
protein, wheat gluten, gelatin, WPIb
obtained from aqueous or

ethanolic solution
Wheat (gluten)
obtained from aqueous solution
biodegradable
reduces moisture loss
adds nutritional value
does not require support
matrix
effective oxygen barrier at low
relative humidity
* high gluten content
* increased puncture strength
and extensibility
more permeable to water

vapor than lipid barriers
vapor barrier ability limited

high gluten content may also
be a disadvantage for those
intolerant to gluten
Polysaccharide Barriers (Baldwin and others 1995)

Pectin
most effective on low moisture products generally made from low-methoxyl
pectin, calcium chloride (cross-l
inker), a plasticizer, and
sometimes organic acids
Chitosan
Nutri-Save (NovaChem) used for
methylation of the chitosan
whole apples and pears
polymer results in increased
resistance to CO2 permeability
use of chitosan with lipids may
solve moisture barrier problems
Derivatives of cellulose
used mainly for composite
Tal Pro-long (Courtaulds Group)
coatings comprised of the sodium
Semperfresh (Surface
salt of carboxymethyl cellulose
Systems Intl, Ltd.)
(CMC) as the film former, with
sucrose fatty acid ester as the
emulsifiers
Carrageenan Coatings
sucessfully used on cut grapefruit
halves (Bryan 1972)
not yet approved by FDA for coatings
can retard water loss from food not adequate moisture

can improve handling and
barriers
appearance of foods
low oxygen permeability
natural preservative, inhibits

growth of fungi
impermeable to gases at
70% RHc
good film formers due to

linear structure of polymer
backbone
O2 is limited in entering the fruit
more than CO2 is from escaping;
limiting buildup of harmful CO2
and maintenance of reduced O2
extracted from several species can reduce moisture loss,
of red seaweeds and used in food oxidation or disintegration of the
systems as a gel
product
a See glossary for definition of molding techniques.

b Wheat protein isolate.
cRelative humidity.
150
* at 100% RH, permeability

to CO2 and O2 due to
diffusion with water
not good barriers to movement

of water; however, the film can
retain a moisture layer which
will delay moisture loss from
the fruit by being the first layer
of moisture lost
not yet approved by the FDA
for food coatings

Table IV-6Edible coating applications and functions 1
Type of edible coating
Polysaccharide coatings
Function
Reference
I. Cellulose
Carboxymethyl cellulose
Bananas
Apples
Fresh fruits and vegetables
Freshly-cut celery
Pears
Tomatoes
Oranges
O2 and CO2 barrier

O2 and CO2 barrier
O2 and CO2 barrier
Moisture barrier
O2 and CO2 barrier
O2 and CO2 barrier
O2 and CO2 barrier
Banks 1984
Banks 1985;
Drake and others 1987
Lowings and Curts 1982
Mason 1969
Meheriuk and Lau 1988
Nisperos and Baldwin 1988
Nisperos-Carriedo and others 1990
II. Starch
Dextrins (starch hydrolysates)
Freshly sliced apples
O2 barrier
Murray and Luft 1973
III. Seaweed Extracts

Carrageenan
Cut grape-fruit halves
Moisture barrier
Bryan 1972
IV. Chitin/Chitosan
Apples, pears, peaches, plums
Fresh strawberries
Fresh cucumbers, bell peppers
O2 and CO2 barrier

Postharvest decay control
Postharvest decay control
Davies and others 1989; Elson and Hayes 1985

El Ghaouth and others 1991a
El Ghaouth and others 1991b
Moisture and O2 barrier
Park and others 1994
Protein Coatings
I. Corn Zein
Zein
Tomatoes
II. Casein
Casein-acetylated monoglyceride
Zucchini
Apples and celery sticks
Casein-stearic acid, beeswax, or acetylated
Peeled carrots
Moisture barrier
Moisture barrier
monoglyceride
Moisture retention
Avena-Bustillos, Krochta, and others 1994

Avena-Bustillos and others 1997
Avena-Bustillos and others 1993, Avena-Bustillos,
Cisneros-Zevallos and others 1994
1 (Adapted from Table IV-3 and Table IV-4 in Krochta and De Mulder-Johnston 1997).
tuce and soybean sprouts. Although inhibition of E. coli and S.

aureus was not measured on the commodities, it was noted that
incorporation of 1.0% GFSE into the LDPE film decreased the
growth rates of aerobic bacteria and yeasts (initial counts ranging
from 103 to 104 CFU/g) over 8 days for the curled lettuce stored at
5 C (59 F). Soybean sprouts were found to have a higher initial
load of aerobic bacteria and yeasts than the curled lettuce (10 6
CFU/g). Therefore, the only observed decrease in growth rates was
for the lactic acid bacteria over a 12-day period at 5 C (41 F).
Further tests need to be performed using this film technology to
ascertain the effects on pathogens as well as aerobic bacteria and
yeasts when the film is used with a food product. Inhibition of
nonpathogenic organisms that can be indicators of organoleptic
quality may lengthen shelf life such that outgrowth of pathogens is
possible, while the product is still organoleptically acceptable.
Grapefruit seed extract is reported to be inhibitory to a number of
human pathogens. There has been evidence, however, that any
antibacterial activity of commercial preparations is due to the various preservative agents (triclosan, methyl parabene, benzethonium chloride) contained within the product. Researchers have
found that products not containing any preservatives and several
self-made preparations had no antimicrobial activity (Woedtke
and others 1999). In the aforementioned study by Lee and others
(1998), the composition of the GFSE incorporated in the film was
not discussed or examined. It is obvious that if pure GFSE is to be
used, its antimicrobial properties will have to be fully investigated.
If the active antimicrobial ingredients in commercial GFSE preparations are preserving agents, they may be better targets for inves-
tigation.
At present, the area of edible films and antimicrobial edible
films is not considered a priority by industry due to overall public
perception and hesitation about adding more chemicals, natural
or not, to fresh produce. Besides the waxing of fruits, edible films
are not commonly used and presently, the main issue involves the
production of coatings with good surface tension that will stick to
produce.
2. Factors affecting shelf life

A main aim of MAP is extension of shelf life. It must be reiterated here that extension of product shelf life may allow outgrowth
and/or growth of pathogens to higher levels as compared to airstored samples. Since fruits and vegetables are still alive and
therefore respiring when harvested and processed, there are
many factors that affect the postharvest shelf life extension of fresh
produce and the success of MAP.
The rate of respiration of a fruit or vegetable is inversely proportional to the shelf life of the product; a higher rate decreases shelf
life (Day 1993; Lee and others 1995). In general, those products
with increased wounding, as in the case of fresh-cut produce, will
have a high degree of perishability due to increased respiration
rates. Respiration can be measured by the oxygen uptake or by
production of CO2 and also results in the production of heat and
water vapor (Zagory 1995). Therefore, a goal of MAP is to decrease the produce respiration rate, which can be successfully
achieved with decreased O2 levels (1-5%) and refrigeration. How-
151

ever, O2 concentrations below 1-2% can lead to anaerobic respiration and the production of off-odors, as well as create ideal conditions for pathogens such as C. botulinum. As previously discussed, high O2 (70-100%) combined with CO2 for MAP has
been tested and shown to have beneficial effects on product quality (Amanatidou and others 1999); however, more research is required to support and explain this concept (Wszelaki and Mitcham 2000; Kader and Ben-Yehoshua 2000).
The delay of senescence, the natural form of deterioration, is the
main goal in the preservation of fresh produce, as senescence accounts for the majority of postharvest losses (Lee and others 1995).
Senescence is endogenously controlled and is the stage when extensive catabolic reactions occur, resulting in dissolution of plant
membranes. It is marked by chlorophyll loss, decreases in RNA and
protein content and tissue softening. Plants, for example, senesce to
reroute materials into seeds representing the next generation; it is
therefore a predestined apoptosis process that can only be delayed,
not completely inhibited. It is driven by an increase in respiration,
as well by an increase in ethylene production in some products, a
process referred to as climacteric. It is therefore reasonable to assume that maintaining and reducing ethylene perception and production may effectively delay senescence.
As mentioned above, ethylene, a plant hormone, plays a large
role in shelf life and can cause a marked increase in respiration
rates and enhance ripening and senescence (Nguyen-the and
Carlin 1994; Day 1993). In some commodities, accelerated ageing and the initiation of ripening can occur following exposure to
ethylene concentrations as low as 0.1 ml/l (Lee and others
1995). As senescence begins, spoilage due to indigenous bacteria
can be augmented. Ethylene is also a by-product of the aerobic
combustion of hydrocarbons, and it is therefore important during
the handling of produce to maintain low levels of environmental
ethylene, which are often increased by fork lifts and other machinery (Zagory 1995). Different biological structures of assorted
produce varieties contribute to the products sensitivity response
to ethylene, as well as the response to O2 and CO2. Furthermore,
different stages of maturity, cultivar and postharvest storage conditions also influence sensitivity to ethylene (Lee and others 1995).
Control measures taken to minimize perception and production
of ethylene following harvest include storage in a modified atmosphere at optimal low temperatures (just above the chilling or
freezing injury threshold) and oxidizing the ethylene by various
chemical and physical means. Part of the success of MAP, and the
quality attributed to MAP products, depends on preventing the
damaging effects of exposure to ethylene. To this end, CO2 can inhibit ethylene action as well as autocatalytic production of ethylene by climacteric products such as apples and tomatoes. However, increased damage to whole leaf plants has been observed at
CO2 levels above 15-20%, thus reinforcing the importance of designing a specific MAP for each product (Lee and others 1995).
Successful control of both product respiration and ethylene
production and perception by MAP can result in a fruit or vegetable product of high organoleptic quality; however, control of
these processes is dependent on temperature control. Along the
whole food continuum, that is, processing, storage, transportation
and retailing, one needs to maintain optimum temperatures.
Maintaining proper storage temperatures is often most difficult at
the retail level, due to the increased handling and the need to
make the product visually appealing. A study by LeBlanc and others (1996) revealed the extent of temperature abuse of produce in
the retail setting. Of 746 and 745 produce samples examined during the winter and summer, 87% and 93% of samples, respectively, that should have been stored at 4 C (39.2 F), were being held
above 4 C (39.2 F) and as high as 8.4 C (47.1 F). Furthermore,
temperature fluctuations between items stored in different parts of
the cabinet were observed. The authors stated that MAP products
152
should probably not be stored with fresh fruit and vegetables. For
some products, the success and microbiological safety of MAP is
dependent on controlled low temperature storage and the products characteristics. Many MAP fresh-cut products overtly spoil
before becoming microbiological safety concerns and thus, the
risk factors, that is, outgrowth of pathogens, for both the upper
and lower limits of recommended storage temperatures for MAP
produce, should be carefully considered when designing a MAP
system. Hintlain and Hotchkiss (1987) presented the concept of a
safety index where products that result in an increasing ratio of
spoilage organisms to pathogenic organisms can be considered
less hazardous than products that show a decrease in spoilage organisms with respect to pathogens. This concept could be used
when designing MAP systems, with a better understanding of the
interaction between spoilage organisms and fresh-cut produce.
State of the art temperature control cabinets are currently being
used at the retail level; however, it is a matter of recovery on invested capital and managing the system. Recent advances in the
cold-storage industry show promise for improved temperature
control of produce during transport as well as at the retail level.
Freshloc Technologies, Inc. recently revealed a state-of-the-art,
wireless, Internet-based data collection system for the transportation of temperature sensitive products. This system automatically
monitors and alerts grocery industry personnel to fluctuations in
storage temperature and can be adapted to the grocery, restaurant
or transport industry. This system should help in maintaining consistent storage temperatures; however, it cannot resolve the problems associated with cabinet design (temperature fluctuations), or
the efforts of grocery personnel to make displays as attractive as
possible, while neglecting recommended storage temperatures.
Mild abuse temperatures will not only shorten product shelf life,
but will also allow for the more rapid growth of psychrotrophic
pathogens in some products.
3. Influence of MAP/CAS on growth and survival of

organisms on produce
3.1. Spoilage organisms
The commonly encountered microflora of fruits and vegetables

are Pseudomonas spp., Erwinia herbicola, Flavobacterium, Xanthomonas, Enterobacter agglomerans, lactic acid bacteria such as
Leuconostoc mesenteroides and Lactobacillus spp., and molds
and yeasts (Nguyen-the and Carlin 1994; Zagory 1999). Although
this microflora is largely responsible for the spoilage of fresh produce, it can vary greatly for each product and storage conditions.
Temperature can play a large role in determining the outcome of
the final microflora found on refrigerated fruits and vegetables,
leading to a selection for psychrotrophs and a decrease in the
number of mesophilic microorganisms. Previous studies have
shown that cabbage (in coleslaw) deteriorated at the same rate at
7 C (44.6 F) and 14 C (57.2 F); however, at 7 C (44.6 F), the
reduction in the total microbial load was significant (King and others 1976). Similar phenomena have been reported for shredded
chicory salads (Nguyen-the and Prunier 1989) and shredded carrots (Carlin and others 1989), where the total counts of the mesophilic flora decreased with temperature. Low temperature storage
not only decreases the growth rate of foodborne pathogens but
also increases the inhibitory effects of MAP by increasing the solubility of CO2 in the liquid phase surrounding a food.
The effect of MAP on lactic acid bacteria can vary depending
on the type of produce packaged. The increased CO2 and decreased O2 concentrations used in MAP generally favor the
growth of lactic acid bacteria. This can expedite the spoilage of
produce sensitive to lactic acid bacteria, such as lettuce, chicory
leaves and carrots (Nguyen-the and Carlin 1994). The effect of

MAP on yeasts is negligible, however, molds are aerobic microorganisms and therefore CO2 can cause growth inhibition at concentrations as low as 10% (Molin 2000), although the effect is not
fungicidal (Littlefield and others 1996). Beuchat and Brackett
(1990a) examined the effects of cutting, chlorine dip and modified
atmospheres on the growth of yeasts and molds on lettuce. At
10 C (50 F), in both air and a modified atmosphere (3% O2 and
97% CO2), and with or without chlorine treatment, the organisms
grew slowly regardless of the conditions and at 5 C (41 F), the
growth over a 15-day period was erratic. However, no specific inhibitory effects of the modified atmosphere were noted.
The concern when using MAP for fruit and vegetables arises
from the potential for foodborne pathogens, which may be resistant to moderate to high levels of CO2 ( 50%), to outgrow spoilage microorganisms, which may be susceptible to the modified
atmosphere (Bennik and others 1998). The interaction of the
pathogenic and resident (saprophytic) microflora has been extensively reviewed for meat and milk products; however, data are still
required for MAP fruits and vegetables (Nguyen-the and Carlin
1994). This interaction of the resident microflora and pathogenic
organisms on MAP produce needs to be studied more extensively
(Francis and OBeirne 1998).
3.2. Pathogenic organisms
There are many steps involved along the whole farm to fork
produce chain and, therefore, many points for potential microbial
contamination (NACMCF 1999). Preharvest contamination of
fresh produce can occur through the use of non-pasteurized manure for fertilization, fecal contamination by indigenous or domestic animal species as well as agricultural workers, contaminated irrigation water, and general human handling (see Chapter I).
During harvest and postharvest, critical points for contamination
include contaminated wash water or ice, human handling, animals, contaminated equipment or transportation vehicles, crosscontamination, and inefficient processing of the product that fails
to remove substantial levels of bacteria (NACMCF 1999).
Therefore, MAP produce is vulnerable from a safety standpoint
because modified atmospheres may inhibit organisms that usually
warn consumers of spoilage, while the growth of pathogens may
be encouraged. Also, slow growing pathogens may further increase in numbers due to the extension of shelf life. Currently,
there is concern with the psychrotrophic foodborne pathogens
such as L. monocytogenes, Yersinia enterocolitica and Aeromonas hydrophila, as well as nonproteolytic C. botulinum, although
clearly a number of other microorganisms, especially Salmonella
spp., E. coli O157:H7 and Shigella spp., can be potential health
risks when present on MAP produce.
3.3. Clostridium botulinum
The spores of C. botulinum are commonly found in agricultural

soils and on the surfaces of fruits and vegetables. Proteolytic C.
botulinum has difficulty growing and producing toxin at temperatures below 12 C (53.6 F), pH below 4.6, a water activity below
0.95 and NaCl concentrations above 10% (Lund and Peck 2000).
Nonproteolytic C. botulinum can grow at a minimum of 3 C
(37.4 F), pH above 5.0, water activity above 0.97 and NaCl concentrations above 4%. Therefore, there is some concern about the
use of MAP with respect to this organism (Zagory 1995). Depending on the product in a MA package, the level of O2 can decrease
rapidly if the product is temperature abused and product respiration increases, leaving a highly anaerobic environment ideal for
the growth and toxin production of C. botulinum (Francis and
others 1999). In a study looking at this potential in lettuce, cabbage, broccoli, carrots, and green beans packaged under vacuum
or in air, Larson and others (1997) found that most often the product was grossly spoiled before significant toxin production was
detected (Table IV-7). The probability of botulinal toxin being produced before the product was obviously spoiled was less than 1
in 105 in the foods examined using the standard mouse assay for
detection of botulinal toxin. Hao and others (1998) found similar
results for shredded carrots and green beans packaged under 4
different films allowing for different oxygen transmission rates.
Similar results were obtained by Petran and others (1995) for romaine lettuce and shredded cabbage; that is, all toxin-positive
samples were grossly spoiled prior to toxin detection. Larson and
Johnson (1999) obtained the same results in a similar study when
looking at the incidence of botulinal toxin production on artificially inoculated cantaloupe and honeydew. At abusive temperatures, with the exception of UV-treated samples, samples were obviously spoiled, although they were also considered marginally
organoleptically unacceptable when toxin was detected. These
findings were supported by the results of Hao and others (1998),
which showed that packaged lettuce and cabbage became
spoiled before becoming toxic. The study by Larson and Johnson
(1999) demonstrated the ability of the spoilage flora to protect
against pathogen overgrowth. It is likely, however, that product
characteristics such as water activity, pH, respiration rate, initial
spore levels, and indigenous microflora play a role in the survival
and persistence of the pathogen on MAP produce. For example,
in 1987, four circus performers in Sarasota, FL became ill with
symptoms of botulism after consuming coleslaw prepared from
packaged shredded cabbage purchased three weeks earlier in
New Orleans (Solomon and others 1990). Researchers suspected
that the cabbage had been packaged using MAP and that contaminated cabbage further contaminated the dressing, leading to
the recovery of C. botulinum type A toxin and spores from the
dressing. A follow-up study done to determine the possibility of C.
botulinum surviving on cabbage in MAP was undertaken, and results indicated that only C. botulinum type A grew and produced
toxin in the modified environment when stored at room temperature (Solomon and others 1990). Two isolates used in the followup study were obtained when the outer leaves of 88 cabbages
were surveyed; 12 of them (13.6%) were found to contain toxin
type A strains. However, this high incidence of type A spores may
have been due to the origin of this particular product and type of
soil. For example, Lilly and others (1996) found that only 0.3% (1
of 337) of sampled shredded cabbage obtained from retail suppliers in the United States contained C. botulinum. However, the
products tested had all been stored at 4 C (39.2 F), below the
minimum for growth of proteolytic C. botulinum.
Growth and toxin production of C. botulinum before obvious
product spoilage has also been observed on Agaricus bisporus
mushrooms (Sugiyama and Yang 1975) and potato slices (Dignan
1985). As well, Austin and others (1998) performed challenge
studies using both nonproteolytic and proteolytic strains of C.
botulinum on MAP fresh-cut vegetables and found that samples
of butternut squash (5 C [41 F], 21 days) and onion (25 C [77
F], 6 days) appeared organoleptically acceptable when toxin was
detected. It was also demonstrated that toxin production by C.
botulinum varied with the vegetables tested. Only nonproteolytic
strains growing on butternut squash were capable of producing
neurotoxin at temperatures as low as 5 C (41 F ) in 21 days,
whereas proteolytic strains were able to produce toxin on all vegetables tested (onion, butternut squash, rutabaga, romaine lettuce,
stir-fry and mixed salad), except coleslaw at 15 C (59 F). and
higher (Austin and others 1998).
A mixture of proteolytic strains were able to produce botulinum
neurotoxin on MAP broccoli, stored at 13 C (55.4 F) and 21 C
(69.8 F), however the product was obviously spoiled by the time
toxin was produced (Hao and others 1999). During a study of uninoculated vacuum packaged minimally processed green bell
peppers, Senesi and others (2000) found that after 7 days at refrig-
153
154
1(O 2),
20.8(CO 2)
1 (O2),
20.8 (CO2)
1(O 2)
Air
Air
air
air
air
Air
Air
Air
vaccum70kPa
vaccum70kPa
air
UK
UK
air
air
UK
air
air
vacuum60kPa
vacuum60kPa
UK
UK
UK
70:30
O2:N 2
air
air
vacuum60kPa
vacuum60kPa
air
6-8000
2100
2100
2100
2100
13013
7000
7000
16000
3000
19-22000
32306
20500
20500
36000
9800
Film gas
permeability
(cm3/m2/24h at 23 C)
O2
CO 2
17000
PVCe
6000 cm3/
100in2
-
19000-22000
trays of
with packet
15g NaCl and
sealed with EVAf
100
800 cm3/
100in2
123
6000-8000
vented package
unvented package
3000
9800
80-100
80-100
80-100
Un-known
6000
16544
35175
80-100
80-100
5500-7500
20000-24000
16544
35175
40
vented package
unvented package
3000
9800
a Non-commercial, prepared by researcher.

b P = proteolytic C. botulinum.
C NP = nonproteolytic C. botulinum .
d Commercially obtained.
e Polyvinyl chloride
f Ethylene-vinyl acetate
Tomato
Honeydew
Cantaloupe
Mushroomsa
Chopped cabbagea
Shredded cabbagea
Shredded cabbagea
Chopped cabbagea
Mixed saladd
Mixed saladd
Mixed saladd
Shredded cabbagea
Lettuce a
Broccoli a
Stir-fry d
Stir-fry d
Green beana
Green beana
Romaine lettuced
Romaine lettucea
Romaine lettuce a
Lettuce a
Carrot a
Butternut squash a
Butternut squash a
Rutabaga a
Broccoli a
Broccoli
Broccoli
Broccoli
Carrot a
Onion a
Product
Initial
modified
atmosphere
1.6
21.6
52
20-60
2
1
39.0
45.8
35.0
-
10
10
17.7
24.2
25.2
10
81.5
22.6
64.7
25.3
10
10.59
13.47
7.16
-
1-2
1.0
0.0
0.0
-
<2
<2
0
0
1.37
<2
0.67
1.10
1.10
0.97
<2
3.68
1.3
1.34
-
Final
modified
atmosphere
O2 (%) CO 2 (%)
P & NP,4100
P & NP, 100
P & NP, 100
P 104/mushroom
P & NP,100/g
P & NP, 100/g

P & NP, 100/g
P & NP,100/g
P 100/g
NP 1000/g
NP 1000/g
P 96-184/g
P & NP, 100/g
P & NP,100/g
P 100/g
P 10/g
P & NP, 100
P & NP, 100
P 100/g
P & NP, 100/g
P & NP, 100/g
P & NP, 100/g
P & NP,100/g
1000/g
NPc 1000/g
P 100/g
P 100/g
P & NP,100/g
P, 102/g
P, 102/g
P, 102/g
P & NP,100/g
Pb
Challenge
level
13
15
7, 15
20
21
21
21
21
25
25
15
22-25
21
12
25
15
21
21
25
21
21
21
21
25
5
25
25
12
13
21
21
21
Temp.
(C)
42-46
No Toxin
NoToxin
No Toxin
10
NoToxin
7
4
14
4
9
11
21
7No toxin
7No toxin
9
28
17
6
4No Toxin
6
21
3
7
9
21
10
10
4No Toxin
Days to
toxin
production
(d)
Table IV-7Conditions supporting growth and toxin production by Clostridium botulinum on fresh-cut MAP produce
Not acceptable
Not acceptable
Inedible 6-9 days
Fair
Spoiled 3d
Inedible
Extensive decay
Spoiled 3d
Extensive decay
Moderate browning
Moderate browning
Acceptable
Gross spoilage
Gross spoilage
Soft
Soft
Grossspoilage
Gross spoilage
Extensive decay
Extensive decay
Entensive decay
Gross spoilage
Gross spoilage
No change,swelling
Decay
Gross spoilage
Spoiled
Spoiled
Spoiled/poor
Gross spoilage
No change,swelling
Appearance
Hotchkiss and others 1992
Larson and Johnson 1999
Larson and Johnson 1999
Sugiyama and Yang 1975
Larson and others 1997
Petran and others 1995

Austin and others 1998

Solomon and others 1990


Hao and others 1999
Hao and others 1999
Hao and others 1999
Reference

eration temperatures, the environment within the package had become anaerobic and high in CO2, stressing the importance of
careful selection of a MAP film and initial gas atmosphere.
Fresh mushrooms and tomatoes have also been shown to contain spores of Clostridium spp., and therefore the possibility of botulism associated with these MAP products must not be ignored
(Zagory 1995). However, it is thought that the acidic nature of tomatoes (pH <4.6) does not provide ideal growth conditions for C. botulinum. This theory was supported by the results of Hotchkiss and
others (1992) who demonstrated that MAP (1.0-2.9% 9). tomatoes
stored at 13 C (55.4 F) and 23 C (69.8 F) became toxic only after becoming severely spoiled, well beyond the point of being organoleptically acceptable. The initial concentration of O2 used for
high respiring products such as mushrooms can be very important
since it will decrease more quickly, resulting in an anaerobic environment. Also, reducing substances of mushrooms can contribute
to a lowering of the oxidation-reduction potential to levels suitable
for bacterial anaerobic growth. The primary reason for toxin production, however, is the low O2 concentration (Sugiyama and
Yang 1975). The standard industry practice of placing holes in the
packaging film can discourage the growth of C. botulinum, although the shelf life of mushrooms is reduced.
A comprehensive survey of 1,118 packages of MAP vegetable
products from three large U.S. cities found an overall incidence
rate of 0.36% of C. botulinum type A spores (Lilly and others
1996). The absence of outbreaks of botulism linked to MAP produce indicates that C. botulinum may be competitively inhibited
under the packaging and resident flora conditions of these products. However, more research needs to be done to examine the
potential for growth of C. botulinum in a wide variety of MAP produce stored at mildly abusive temperatures such as 7-12 C (44.6
to 53.6 F) . In addition, other hurdles besides temperature need
to be examined to prevent botulinum toxin production.
3.4. Listeria monocytogenes
Recently, concerns about possible pathogen contamination in

MAP produce have focused on L. monocytogenes due to its ability to grow at refrigeration temperatures (NACMCF 1999). Numerous researchers have reported that this organism can remain
largely unaffected by MAP, while the normal microflora is inhibited (Amatanidou and others 1999; Francis and OBierne 1997,
1998). Thus, although MAP produce can remain organoleptically
acceptable, L. monocytogenes, with a reduced microflora and, especially if low levels of lactic acid bacteria are present, can grow
at low temperatures to potentially harmful levels during the extended storage life of a MAP produce product.
Early studies showed that L. monocytogenes inoculated onto
broccoli, asparagus and cauliflower was unaffected by a modified
atmosphere of 3% CO2, 18% O2 and 79% N2 for 10 days at
10 C (Berrang and others 1989a). Further studies by Beuchat and
Brackett (1990a) clearly demonstrated that L. monocytogenes increased significantly in number on lettuce stored in a modified atmosphere of 3% O2 and 97% N2. Ringl and others showed that
L. monocytogenes did not grow on shredded lettuce stored at either 4 C (39.2 F) or 8 C (46.4 F) when packaged under air using a semipermeable film, but did grow on the same product
when flushed with nitrogen (Francis and OBeirne 1997). Francis
and OBeirne (1997) also reported that the growth of L. monocytogenes was stimulated by nitrogen flushing at 8 C (46.4 F). In
addition, increasing CO2 levels from 10 to 20% has been reported to stimulate the growth of L. monocytogenes in a surface model system (Amanatidou and others 1999).
Challenge studies conducted by Farber and others (1998) focused on commercially available packaged vegetables and salads, as well as vegetables processed to mimic foodservice conditions. The importance of refrigeration was clearly demonstrated as
L. monocytogenes population levels remained constant on all

fresh-cut, processed and packaged vegetables stored at 4 C (39.2
F), with the exception of butternut squash and carrots on which
the levels increased and decreased, respectively. At 10 C (50 F),
the growth of L. monocytogenes was supported on all vegetables
tested with the exception of chopped carrots, where the population decreased by 2 log units over 9 days. The inhibitory properties of raw, uncooked carrots and carrot juice on the growth of L.
monocytogenes have been previously reported (Beuchat and
Brackett 1990b). As well, Jacxsens and others (1999) reported a
decline in L. monocytogenes on both Brussels sprouts and carrots
packaged under a modified atmosphere (2 to 3% 9). 2 to 3%
CO2, and 94 to 96% N2) and stored at 7 C (44.6 F),. Under severe temperature abuse conditions (25 C [77 F], for 1-2d) followed by storage at 4 (39.2 F) or 10 C (50 F), inoculated Caesar
salad and coleslaw mix supported the growth of L. monocytogenes, although larger increases were noted for the coleslaw mix.
These results support those of Beuchat and Brackett (1990a), who
found that L. monocytogenes could grow on lettuce following
commercial processing procedures such as chlorine treatment,
modified atmosphere and shredding. Jacxsens and others (1999)
investigated the behavior of L. monocytogenes and Aeromonas
spp. on minimally processed vegetables packaged under either a
modified atmosphere (that is, 2-3% 9). 2-3% CO2, 94-96% N2) or
air, and found that the organoleptic quality of the produce was
obviously decreased before pathogen levels increased significantly, and that the growth of the psychrotrophic pathogens was influenced more by the type of vegetable than the atmosphere used.
This phenomenon was also observed for L. monocytogenes inoculated on minimally processed green salads; that is, growth was
faster on butterhead lettuce than on green endive and was not observed on lambs lettuce (Carlin and Nguyen 1994). These observations could also be linked to the varied sensitivities of different
produce to MAP conditions which can accelerate tissue senescence and death, thus providing nutrients for growth of the pathogens; however, the organoleptic quality of the lettuce was not noted by Carlin and Nguyen (1994). Both carrots and Brussels
sprouts demonstrated inhibitory activity towards Listeria (Jacxsens
and others 1999). In general, Aeromonas grew faster than L.
monocytogenes on shredded chicory endives and shredded iceberg lettuce, consistent with previously reported growth rates on
refrigerated vegetables (Anonymous 1996). Castillejo Rodriguez
and others (2000) performed a similar study looking at the growth
of L. monocytogenes on trimmed fresh green asparagus stored
under air. Populations decreased at 2 C (35.6 F) and 4 C (39.2);
however, at 8 C (46.4 F), they increased at a rate of 0.038/hour.
A modified atmosphere developed in the package with an increase in the levels of CO2 (1.63-15.63% at 8 C [46.4 F], 528
hours) and a decrease in O2 (18.13-10.35% at 8 C [46.4 F],
528 hours). These conditions did not affect the growth of L.
monocytogenes, and the authors concluded that these conditions
might allow L. monocytogenes to reach potentially hazardous levels during the shelf life of the product. As with other studies (Garcia-Gimeno and others 1996), only temperature had a significant
influence on the growth of L. monocytogenes, and storage temperatures below 4 C (39.2 F) were required to maintain the safety of the product.
The effects of competition between the indigenous microflora
and pathogens on MAP produce have not been studied extensively. However, in a recent study, Francis and OBeirne (1998) used a
surface model agar system to examine the effects of storage atmosphere on L. monocytogenes and the competing microflora
(Pseudomonas fluorescens, P. aeruginosa, Enterobacter cloacae,
Enterobacter agglomerans and Leuconostoc citreum). The findings
suggested that MAP conditions (5-20% CO2, balance N2 and 3%
O2) might increase the growth rate of L. monocytogenes. They did
155

find that at increased CO2 levels (20%), the growth of the lactic acid
bacteria increased, inhibiting the growth of the pathogen, possibly
due to the production of well-known antilisterial agents.
Pseudomonads had no effect on the growth rate of L. monocytogenes in this study, although the fluorescent pseudomonads have
been previously shown to activate the growth of L. monocytogenes
in various foods, a phenomenon related to the release of potential
nutrients by the pseudomonads (Liao and Sapers, 1999; Nguyen-the and Carlin, 1994). Alternatively, Liao and Sapers (1999)
also reported that P. fluorescens strains inhibited the growth of L.
monocytogenes on endive leaves and spinach, possibly due to
the production of a fluorescent siderophore by the
pseudomonads. In general, at 3% 9). a level often reached in
commercial MAP packages, it appeared that growth of the inoculated mixed natural population was decreased, whereas L. monocytogenes proliferated.
Reports of L. monocytogenes growing on sliced apples in controlled atmosphere (Conway and others 1998) and peeled potatoes in vacuum-packages (Juneja and others 1998) at abusive
temperatures provide further evidence that this organism may
pose a safety risk with respect to certain MAP fruit and vegetable
products, and reiterates the importance of Good Agriculture Practices (GAP), Good Manufacturing Practices (GMP) and HACCP for
produce postharvest handling and processing.
More research needs to be done to examine the influence of
different atmospheres, background microflora and storage temperatures on the survival and growth of L. monocytogenes on
MAP fresh-cut produce.
3.5. Aeromonas hydrophila
Aeromonas spp. can be found on a wide variety of foods, as

well as in most aquatic environments and most often causes gastroenteritis, and occasionally septicemia (Kirov 1997). Additional
information regarding pathogenesis may be found in Chapter III.
Similar to L. monocytogenes, A. hydrophila can grow at refrigeration temperatures, and several studies have shown that growth is
not affected by low O2 levels (1.5%) and CO2 levels up to 50%
(Francis and others 1999). A survey of 97 prepared salads found
A. hydrophila to be present in 21.6% of them, significantly lower
than in meat products tested (Fricker and Tompsett 1989). Hudson and De Lacy (1991) also did a small survey of 30 salads and
found A. hydrophila in only one salad package not containing
mayonnaise. They surmised that the mayonnaise lowered the pH
of the food, thereby inhibiting the growth of or inactivating the
aeromonads present. Differences in recovery rates between the
studies of Fricker and Tompsett (1989) and Hudson and De Lacy
(1991) may be due to methodology. Fricker and Tompsett (1989)
tested three solid media for recovery of Aeromonas spp. and may
have subsequently achieved better recovery, as compared to
Hudson and De Lacy (1991) who only used one plating medium.
Garcia-Gimeno and others (1996) observed a decline in bacterial
numbers paralleled by a decrease in pH and increase in CO2, for
A. hydrophila inoculated vegetable salads stored at 15 C (59 F).
At 4 C (39.2 F), the bacteria survived, but did not grow. The actual significance of finding A. hydrophila on foods is unclear at
the present time.
Berrang and others (1989b) determined that although at both
4 C (39.2 F) and 15 C (59 F), the shelf life of broccoli, asparagus and cauliflower was prolonged by MAP (that is, 11-18% 9).
3-10% CO2, 97% N2), it did not negatively affect the growth of
resident or inoculated A. hydrophila. Interestingly, the organism
was detected on most lots obtained from the commercial producer. Therefore, for storage periods of 8-21 days, depending on the
product, A. hydrophila increased from roughly 104 to 108 or 109
CFU/g, and product that appeared suitable for consumption was
heavily contaminated with the pathogen. As with L. monocytoge156
nes, the CO2 levels that were inhibitory to A. hydrophila (that is,
>50%) also damaged the product (Bennik and others 1995). As
previously discussed, the challenge study performed by Jacxens
and others (1999) demonstrated that Aeromonas grew faster than
L. monocytogenes on minimally processed vegetables in air and
MAP and that a decline in the populations of both organisms was
observed on Brussels sprouts . A recent study has proposed the
use of a Lactobacillus casei inoculum combined with MAP and
chill temperatures to reduce the survival and/or growth of A. hydrophila in ready-to-use vegetables such as fresh-cut lettuce (Vescovo and others 1997). Previous studies have shown that an increase in lactic acid bacteria combined with high levels of CO2
(33%) decreases product pH and, therefore, populations of Aeromonas spp. on vegetable salads (Garcia-Gimeno and others
1996). However, the increased level of CO2 could damage the
product.
3.6. Other pathogens of concern with respect to MAP
produce
Organisms such as Salmonella, Shigella, E. coli, and various enteric viruses, such as hepatitis A, have been implicated in produce
outbreaks, and, therefore, there is concern about their behavior
under modified atmosphere conditions (Zagory 1995; Amanatidou and others 1999). A 1986 outbreak of shigellosis was traced
back to commercially distributed MAP shredded lettuce; 347
people were affected in two west Texas counties (Davis and others
1988). Fernandez-Escartin and others (1989) tested the ability of
three strains of Shigella to grow on the surface of fresh-cut papaya, jicama, and watermelon and reported that populations increased significantly when the inoculated product was left at
room temperature for 4 to 6 hours. Shigella is not part of the normal flora associated with produce, but can be passed on as contaminants by infected food handlers and contaminated manure
and irrigation water.
More recently, an outbreak of Salmonella Newport was reported
in the U.K., associated with the consumption of ready-to-eat salad
vegetables (PHLS 2001). To date, nine human cases have been identified with the isolated strain from the implicated salad vegetables
having an identical PFGE pattern to three of the human isolates.
In an agar-based study to investigate the effects of high (8090%) O2 and moderate (10-20%) CO2 concentrations on foodborne pathogens at 8 C (46.4 F), Amanatidou and others (1999)
noted little inhibitory action against a number of pathogens. All
pathogens were able to grow in air; however, S. Typhimurium
grew slowly, at a rate of 0.011 m/h. Ten to 20% CO2 was inhibitory to S. Enteritidis; however, S. Typhimurium, L. monocytogenes
and nonpathogenic E. coli were unaffected or stimulated. Only
when high O2 (90%) and moderate CO2 levels (10-20%) were
used, did consistently strong inhibition of S. Enteritidis and E. coli
occur. Kakiomenou and others (1998) however, found that S. Enteritidis numbers decreased on both carrots and lettuce when
stored under 5% CO2, 5.2% O2 and 89.9% N2. Salmonella Typhimurium and L. monocytogenes actually had an increased growth
rate at these concentrations; growth increased from 0.011 and
0.031 m/h to 0.023 and 0.041 m/h for S. Typhimurium and L.
monocytogenes, respectively. In general, E. coli O157:H7, S. Hadar and S. Typhimurium were only inhibited by CO2 levels that
caused damage and spoilage to the produce (Piagentini and others 1997; Amanatidou and others 1999; Francis and others
1999). A modified atmosphere of 3% O2 and 97% N2 also had
no significant effect on E. coli O157:H7 inoculated onto shredded
lettuce, sliced cucumber, and shredded carrot and incubated at
12 and 21 C (21.6 and 69.8 F) (Abdul-Raouf and others 1993).
At 5 C (41 F), populations of viable E. coli O157:H7 declined
on stored vegetables; however, at 12 and 21 C (53.6 and 69.8
F), populations increased, demonstrating the importance of re-

frigeration temperatures in maintaining product safety. Richert and
others (2000) who, although not studying MAP, reported that E.
coli O157:H7 could survive on produce (broccoli, cucumbers
and green peppers) stored at 4 C (39.2 F) and proliferate rapidly
when stored at 15 C (59 F). In 1993, there were two foodborne
outbreaks of enterotoxigenic E. coli (ETEC) linked to carrots in a
tabouleh salad served in New Hampshire and to an airline salad
on a flight from North Carolina to Rhode Island (CDC 1994). Although these carrots were of U.S. origin, ETEC is a common cause
of diarrheal illness in Mexico and developing countries that import fresh product to North America. Research on the behavior of
this pathogen on fresh and fresh-cut product, both under MAP
and without MAP, seems warranted.
Information on the survival of the enteric pathogens Y. enterocolitica and Campylobacter spp. on MAP produce is extremely
limited, and mainly consists of data involving meat products.
These organisms can be recovered from animal reservoirs as well
as water sources and theoretically, produce may occasionally become contaminated by the application of natural fertilizers, manure, by wild animal feces, or by contaminated surface or irrigation water (Barton and others 1997; Wallace 1997). There is some
evidence that mushrooms may be a source of Campylobacter jejuni; it was isolated from 1.5% of retail, polyvinyl chloride filmwrapped, and fresh mushrooms in 1984 (Doyle and Schoeni
1986). It has been suggested that the mushrooms may become
contaminated by harvesters. Two separate studies looking at store
bought lettuce (Park and Sanders 1992; Little and others 1999) as
well as spinach, radish, green onions, parsley and potatoes (Park
and Sanders 1992) did not find any evidence of Campylobacter
spp., indicating that there may be minimal risk, regardless of the
packaging technology used. Interestingly, Park and Sanders (1992)
found evidence of gross contamination by Campylobacter spp. of
produce at farmers markets, suggesting that industrial processing
may be effective in removing certain pathogens from fresh produce
before retail sale. Alternately, contamination may have occurred at
the market. A Canadian study detected no Campylobacter in any of
65 unprocessed or 296 fresh-cut and packaged ready-to-use vegetables such as lettuce, carrot, cauliflower, celery, broccoli, or sliced
green peppers (Odomeru and others 1997). A more recent study,
investigating the survival of C. jejuni on MAP fresh-cut cilantro and
lettuce, found that refrigeration temperatures in combination with a
modified atmosphere of 2% O2, 18% CO2 and 80% N2 can be favorable for bacteria (Tran and others 2000). Due to the microaerophilic nature of Campylobacter spp., which require 5% O2, 10%
CO2 and 85% N2 for optimal growth, the investigators suspected
that a low O2 modified atmosphere may provide an environment
conducive to survival of the pathogen. Campylobacter jejuni (initial
level 106 CFU/g) was able to survive on cilantro, green pepper, and
romaine lettuce packaged under normal air, modified atmosphere,
and vacuum, for 15 days of storage at 4 C (39.2 F). After 9 days of
storage at 4 C (39.2 F) C. jejuni levels decreased to approximately
104 CFU/g on all three vegetables stored under the modified atmosphere. In contrast, C. jejuni decreased to levels of approximately
102 and 103 CFU/g for all vegetables packaged under normal air
and vacuum, respectively.
Studies to determine the behavior of Y. entercolitica on MAP
produce have not been published, however data obtained with
meat products indicate that 40-50% CO2 has minimal inhibitory
effects on its growth (Francis and others 1999).
Enteric viruses such as Norwalk and hepatitis A (HAV) are often
the cause of very large foodborne outbreaks, yet none have been
linked specifically to MAP produce, and only HAV has been
linked to outbreaks involving fresh produce (Beuchat 1996). Of
14 reports of viral gastroenteritis cited by Hedberg and Osterholm, salad was implicated as the vehicle in 36% (Beuchat 1996).
One of the HAV outbreaks was linked to the consumption of
commercially distributed lettuce that was washed, sliced and

bagged before being distributed to restaurants in Kentucky
(Rosenblum and others 1990). A total of 202 people were affected, and the investigation suggested that contamination occurred
before distribution to the restaurants. Most often these viruses are
transmitted by an infected food handler, through the fecal-oral
route. In a survival study, lettuce inoculated with HAV was stored
in normal air as well as various MAP conditions at both 4 C
(39.2 F) and room temperature (Bidawid and others 2001). The
highest rate of virus survival on washed lettuce stored at 4 C
(39.2 F) for 12 days, was observed for product stored under 70%
CO2:30% N2 and 100% CO2, (that is, 83.6 and 71.6%, respectively). Virus survival was significantly lower at room temperature,
which was decreased slightly by the addition of CO2 (that is, >
70%), and the lowest virus survival rate (47.5%) was on lettuce
stored in a petri dish under air. It should be noted that these CO2
concentrations would be harmful to the product and are not used
in retail. These results are consistent with those of Bagdasaryan
(1964), who studied the survival of enteroviruses on radishes, tomatoes, and lettuce stored at 6 to 10 C (42.8-50 F) for periods
exceeding the normal shelf life of these products, as well as with
those of Badawy and others (1985), who studied the survival of
rotavirus on lettuce, radishes, and carrots stored at 4 C (39.2 F)
and room temperature. In all these studies, the greatest survival
rates were observed at refrigeration temperatures. Studies to determine the role of the competitive bacterial microflora on virus survival may be beneficial.
The protozoan parasites Cyclospora cayatenensis, Cryptosporidium parvum and Giardia lamblia have been the etiologic
agents in serious foodborne outbreaks involving berries (Herwaldt
2000), apple cider (Millard and others 1994; CDC 1997), and raw
sliced vegetables (Mintz and others 1993), respectively. The behavior of these organisms under MAP is not known. However, the
increase in incidence of produce-linked outbreaks due to these
organisms indicates that research in this area is necessary. Research is needed to examine the behavior of both foodborne viruses and protozoan parasites on MAP produce.
To date, only two MAP produce products, coleslaw mix (Solomon and others 1990) and ready-toeat salad vegetables (PHLS
2001), have been implicated in foodborne illness outbreaks of
botulism and Salmonella Newport, respectively. As well, although
it is unclear how the product was packaged, commercially distributed shredded lettuce caused an outbreak of shigellosis in the
United States in 1986 (Davis and others 1988). There has been a
noticeable increase in the consumption of fresh fruit and vegetables in the last two decades, and more consumers are choosing
the less labor-intensive fresh-cut produce. There has been a parallel rise in the number of produce linked foodborne outbreaks, but
not linked to fresh-cut produce packaged under MAP. However,
vigilance with respect to the safety of these products must be
maintained.
4. Conclusions
Oxygen, CO2, and N2, are most often used in MAP/CAS.
Among them, CO2 is the only one with a direct antimicrobial effect, resulting in an increased lag phase and generation time during the logarithmic phase of growth. Although other gases such as
nitrous and nitric oxides, sulphur dioxide, ethylene, chlorine, as
well as ozone and propylene oxide have been investigated, they
have not been applied commercially due to safety, regulatory, and
cost considerations.
The recommended percentage of O2 in a modified atmosphere for fruits and vegetables for both safety and quality falls between 1 and 5%, although the oxygen level will realistically reach
levels below 1% in MAP produce.
157

The concern when using MAP for fruit and vegetables arises
from the potential for foodborne pathogens, which may be resistant to moderate to high levels of CO2 (< 50%), to outgrow spoilage microorganisms, which may be susceptible to the modified
atmosphere.
It is generally believed that with the use of permeable films,
spoilage will occur before toxin production is an issue; MAP of
produce, however, should always incorporate packaging materials that will not lead to an anoxic package environment when the
product is stored at the intended temperature.
The background microflora is largely responsible for the
spoilage of fresh produce and can vary greatly for each product
and storage conditions. The elimination or significant inhibition of
spoilage organisms should not be practiced, as their interaction
with pathogens may play an integral role in product safety.
Edible films for use in MAP systems is an active area of research. However, as with other MAP, they can create a very low
O2 environment where anaerobic pathogens such as C. botulinum may thrive. Antimicrobial compounds that can be incorporated into the coating are also being currently investigated.
There have been many studies investigating the migration of
antimicrobials such as sodium benzoate, benzoic acid, propionic
acid, and potassium sorbate from coatings into food. It appears
that the most advantageous use of these films for antimicrobial
properties would be the formation of a monolayer lipid and sorbic acid film, or a bilayer film composed of a hydrophilic base
layer coated with a thin layer of lipid containing sorbic acid. The
main issue involves the production of coatings with good surface
tension that will stick to produce.
Successful control of both product respiration and ethylene
production and perception by MAP can result in a fruit or vegetable product of high organoleptic quality; however, control of
these processes is dependent on temperature control. Along the
whole food continuum, that is, processing, storage, transportation
and retailing, one needs to maintain optimum temperatures.
Maintaining proper storage temperatures is often most difficult at
retail level.
Currently, there is concern with psychrotrophic foodborne
pathogens such as L. monocytogenes, Y. enterocolitica and A. hydrophila, as well as nonproteolytic C. botulinum, although clearly
a number of other microorganisms, especially Salmonella spp., E.
coli O157:H7 and Shigella spp., can be potential health risks
when present on MAP produce.
The success and microbiological safety of MAP is dependent
on controlled low temperature storage and the products characteristics.
Only two MAP produce products, coleslaw mix and ready-toeat salad vegetables, have been implicated in foodborne illness
outbreaks of botulism and Salmonella Newport, respectively.
5. Research Needs
Investigate the antimicrobial effect of superatmospheric O2 in
the fresh-cut produce safety.
Study the interactions of the background microflora with
foodborne pathogens in various modified atmospheres used for
produce, as well as the effects of different gaseous environments
on the survival and growth of bacterial foodborne pathogens on
whole and fresh-cut produce.
Examine the potential for growth of C. botulinum in a wide
variety of modified atmosphere packaging (MAP) produce stored
at mildly abusive temperatures such as 7-12 C. In addition, other
hurdles besides temperature need to be examined to prevent botulinum toxin production.
Examine the influence of different atmospheres, background
microflora, and storage temperatures on the survival and growth
158
of L. monocytogenes on MAP fresh-cut produce.

Investigate the behavior of verotoxin-producing E. coli on
fresh and fresh-cut product, both under MAP and without MAP.
Explore the survival of the enteric pathogens Y. enterocolitica
and Campylobacter spp. and the behavior of foodborne viruses
and protozoan parasites on MAP produce.
Hurdle technology or the combination of novel methods of
food treatment and packaging need to be examined, for example,
irradiation used with MAP and antimicrobial films used in combination with MAP.
Evaluate the use of intelligent packaging systems.
Glossary
Blanketing. The replacement of the air surrounding the contents
of a package with a mixture of atmospheric gases different in proportion from that of air.
Coating. This term as used throughout this text refers to an edible film applied and formed directly on the food product.
Complex coacervation. Where two hydrocolloid solutions with
opposite electron charges are mixed, thus causing interaction and
precipitation of the polymer complex.
Controlled atmosphere. Intentional alteration of the natural
gaseous environment and maintenance of that atmosphere at a
specified condition throughout the distribution cycle, regardless
of temperature or other environmental variations. Normally applied during long term storage and long term distribution (Brody
1989).
Emulsion. Type of edible lipid barrier in which the lipid is uniformly dispersed throughout the edible barrier.
Ethylene Perception. The perception of the presence of ethylene by the plant product. Plants contain protein receptors within
their plasma membranes that may bind to ethylene and trigger a
molecular cascade up regulating many of the genes involved in
ripening, senescence and the biosynthesis of enzymes for in vivo
biosynthesis of ethylene (Gorney; personal communication; unreferenced)
Film. Structure applied to a food product after being formed
separate from that food product. A common term for breathable
flexible packaging materials used to bag produce.
Gelatin or thermal coagulation. Where heating of the macromolecule, which leads to its denaturation, is followed by gelatin
or precipitation, or even cooling of a hydrocolloid dispersion
causing gelatin.
Laminate. Type of lipid barrier where the lipid is a distinct layer
within the edible barrier. May also be used to describe certain
flexible packaging materials which are constructed by binding
dissimilar flexible packaging materials (films) together via an adhesive.
Modified atmosphere. Initial alteration of the gaseous environment in the immediate vicinity of the product, by interactions of
the packaging materials and the produce. The package atmosphere is not static, but will vary depending upon the packaging
materials used, product type, product mass and storage temperature (Brody 1989).
Plasticizer. Compounds added to edible films to decrease brittleness and increase flexibility, toughness and tear resistance.
Those having food applications include mono-, di- and oligosaccharides, polyols, and lipids. Plasticizers such as ethyl vinyl acetate (EVA) are also used in polyethylene film films to alter machinability and oxygen transmission rate (OTR).
Simple coacervation. Where a hydrocolloid dispersed in water
is precipitated or undergoes a phase change after solvent evaporation (drying), after the addition of a hydrosoluble non-electrolyte in which the hydrocolloid is insoluble, after pH adjustment of
the addition of an electrolyte which induced salting out or cross-

linking.
Vacuum packaging. Partial removal of air within the package
without deliberate replacement with another gas (Brody 1989).
Wheat gluten. The water-insoluble proteins of wheat flour composed of a mixture of polypeptide molecules, and considered to
be globular proteins.
Zein. One of the four groups of proteins in corn, which is a prolamine and the only corn protein that is produced commercially;
it is characterized by its ability to form tough, glossy, hard,
greaseproof coatings after evaporation of aqueous alcoholic solutions.
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The author would like to acknowledge Stacey Mantha and Anne Sewell for all the help during the production of this document.

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Chapter IV

these conditions are maintained throughout storage. Examples of

COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETYVol. 2 (Supplement), 2003

Chapter IV: Microbiological Safety of Controlled and Modified Atmosphere Packaging . . .

Table IV-1Commercially available controlled atmosphere

Oxygen Control Systems

External gas generator

Oxygen is removed from incoming air by

modified atmospheres used for produce, as well as on the effects

There are a number of commercially available systems for CAS

Vol. 2 (Supplement), 2003COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY

IFT/FDA Report on Task Order 3

Permeability(cm3/m2.d.atm for 25 mu film at 25 C)

Ethylene-vinyl alcohol (EVOH)

O2 scavengers with O2 indicators

packaging, it will not be discussed further.

MAP is used mainly for wholesale/foodservice use and retail

COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETYVol. 2 (Supplement), 2003

Chapter IV: Microbiological Safety of Controlled and Modified Atmosphere Packaging . . .

Pallet Package System

Pallet box wrapped in heavy gauge polyethylene, with a silicone

Apples, pears and other perishables

MAPAX (AGA, Sweden)

0.75, 1.25, 2.5 mm thick bag made of several layers of

Cabbage in Canada, other perishables

Fresh-cut asparagus, broccoli,

Fresh-cut produce, lettuce,

Broccoli, asparagus, cauliflower and

Spark perforated films which result in non-uniform perforations

Brussels sprouts, lettuce, broccoli,

Cartons with films laminated within the cardboard or coated on

Strawberries, broccoli, and other

Blend of sucrose esters of fatty acids and sodium carboxymethyl

(continued on next page)

IFT/FDA Report on Task Order 3

PacRite products (American Variety of products, water-based carnauba-shellac emulsions,

Apples, citrus, tomatoes, cucumbers,

Apples, citrus and other firmsurfaced fruit

Citrus, apples, stone fruits, pomegranates, tomatoes, pineapple, canta

Activated Earth Films

Typically polyethylene bags with powdered clay material made of

Specific for each product

Fruits and vegetables, coffee

Fruits and vegetables

COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETYVol. 2 (Supplement), 2003

Chapter IV: Microbiological Safety of Controlled and Modified Atmosphere Packaging . . .

some are returnable, and thus reuse is possible in some cases. An

In-store packaging has recently been applied to the new online

Vol. 2 (Supplement), 2003COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY

IFT/FDA Report on Task Order 3

Reproduced from Gorny (1997) by permission of J.R. Gorny.

1.3. Films used in MAP

and edible packaging systems (Guilbert and others 1996; Phillips

COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETYVol. 2 (Supplement), 2003

Chapter IV: Microbiological Safety of Controlled and Modified Atmosphere Packaging . . .

Vol. 2 (Supplement), 2003COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY

IFT/FDA Report on Task Order 3

Lipid-Based Coatings (Koelsch 1994)

non-lipid support matrix required lower water vapor permeability

requires non-lipid support

requires non-lipid support

obtained from aqueous or

obtained from aqueous solution