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Appl Environ Microbiol, January 1998, p. 192-196, Vol. 64, No. 1
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Effect of Inoculation Techniques and Relative
Humidity on the Growth of Molds on the Surfaces of Yellow Layer Cakes
Patrick
Fustier,1,*
Alain
Lafond,2
Claude P.
Champagne,1 and
François
Lamarche1
Food Research and Development Center,
Agriculture and Agri-Food Canada,
St.-Hyacinthe,1 and
Culinar Inc.,
Ste. Marie de Beauce,2 Quebec, Canada
Received 30 January 1997/Accepted 17 October 1997
 |
ABSTRACT |
Four inoculation techniques were compared for initiation of growth
on cake surfaces: spot, air cabinet, spray (atomizer), and talc
addition methods. Molds were isolated from commercial cakes and were
identified as Aspergillus sydowii, Aspergillus ochraceus, Penicillium funiculosum, and
Eurotium herbariorum. Cake surfaces were inoculated with
mold spores and incubated under three equilibrium relative humidity
(ERH) levels: 97, 85, and 75%. Random contamination by spores in a
ventilated air cabinet was the simplest method of
inoculation, but standard deviations in the inoculation
rates (20% on a relative scale) were almost twice those observed with
the other methods. The spot method was the most reproducible. Cake
samples inoculated in the air cabinet had colony counts 10 times lower
than those obtained for potato dextrose agar plates at 97% ERH, which
was not the case with the spray and talc methods. Growth of molds was
much slower in the samples incubated in 75% relative humidity, with
all methods. Colony counts were generally similar in systems adjusted
at 85 to 97% ERH but were lower for samples incubated at 75% ERH. In comparisons of the shelf life estimates obtained by the various inoculation methods, a correlation coefficient
(r2) of 0.70 was obtained between the
spot method and the other methods of inoculation, while talc, air
cabinet, and spray shelf life data were correlated better
(r2 
0.97). The spot method appeared
to be the method of choice in consideration of ease of use, precision,
and the ability to enable the study of the effects of the environment
on mold-free shelf life as well as on the rate of growth of molds on
cakes.
| |
INTRODUCTION |
Yellow layer cakes are bakery
products made from wheat flour, water, vegetable oil, sugar,
emulsifier, eggs, and baking powder. By definition, these cakes contain
almost equivalent amounts of sugar and flour, while whole eggs and
shortening represent 40 and 20 to 40%, respectively, of the content on
a flour basis. Traditionally, these products are packaged in plastic
film after baking, cooling, and the addition of fillings (e.g.,
vanilla) or topping (e.g., chocolate), and they are consumed within 1 month.
As products of intermediate moisture content with abundant nutrients,
these cakes are prone to mold growth. Postprocess contamination is
unavoidable (1, 12, 18), and a wide range of molds, such as
Penicillium, Aspergillus,
Cladosporium, and Eurotium species, gain access
to the product surface prior to packaging. Sporadic appearance of
white, grey, blue, and black molds may limit the product's shelf life
to less than 2 or 3 weeks. Factors such as pH, nutritional profile,
storage temperature, redox potential, addition of either propionate,
sorbate, or benzoate (8), gas packaging involving a
CO2-N2 gas mixture (11, 13), control of headspace oxygen via the use of oxygen absorbents (16),
incubation in ethanol vapor (17), and the relative humidity
(RH) of the atmosphere surrounding the product (3, 6, 14)
all have a bearing on the mold-free shelf life. However, the merits and disadvantages of techniques for inhibition of mold growth need to be
compared via a microbial-inoculation abuse study.
Mold-free shelf life can be assessed by adding a known number of spores
to the product's surface prior to packaging and storage. At least
three artificial inoculation techniques are known: (i) the spot method,
which relies on the properties of mold colonies to grow radially at a
constant rate on solid media and was applied successfully to cheese for
quantification of the kinetics of growth (19); (ii) the
spray method, in which a spore suspension is vaporized on a solid
medium by applying constant pressure on a manual piston (2, 4,
7); and the talc method, in which the colonization is carried out
under a laminar flow hood with mold-contaminated talc (13,
15).
Although various techniques for inoculation of mold onto foods have
been used, their efficiency or appropriateness in abuse studies of
layer cakes has not been determined. Our objective was to examine
various inoculation techniques and the role of environmental RH on the
kinetics of mold growth in determining the mold-free shelf life.
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MATERIALS AND METHODS |
Mold cultures.
Five mold strains were isolated from cakes
provided by the quality control department of Culinar (Ste. Marie de
Beauce, Quebec, Canada). One strain, a darkly pigmented
Mucor-like culture, could not be identified and was coded
CRDA-1. The four other strains were identified and coded as
Aspergillus sydowii CRDA-16, Aspergillus ochraceus CRDA-8, Penicillium funiculosum CRDA-12, and
Eurotium herbariorum CRDA-11.
The strains were propagated on acidified (pH 3.5; 10% tartaric acid)
potato dextrose agar (PDA) (Difco, Detroit, Mich.). Although theoretically a high-pH, low-water-activity (low-aw) medium
would have provided a more representative growth medium, acidified PDA was used since it is recommended for general yeast and mold growth (9). Once abundant growth and spore formation were obtained, generally after 10 to 12 days at 24°C, 10 ml of a sterile 10% NaCl
solution was added to the surface of the agar plates. The spores were
recovered by gentle swirling of the saline solution over the mold
colonies. Spore suspensions of approximately 106 to
109 CFU/ml were obtained by this procedure. The spore
suspensions were stored in 10% saline and maintained at 4°C until
used (within 7 days). No detectable mortality was observed during this
storage period. The spore suspensions were quite stable, as mortality was limited to 0.5 log unit after 7 months of storage at 4°C.
Cakes.
The intermediate-moisture cakes (IMC) used for this
study were typical yellow layer cakes supplied by Culinar.
Commercially, such cakes are used in combination with vanilla fillings
and may be coated with a chocolate blend, but the cakes used for this study did not have such additions. The cakes were produced at a Culinar
plant and shipped within 1 day to the Food Research and Development
Center, Agriculture and Agri-Food Canada, St.-Hyacinthe, Quebec,
Canada. Ingredients included flour, water, vegetable oil, sugar,
emulsifier, eggs, and sodium bicarbonate (see Table 1). Cakes B and C
were chocolate flavored, while cake A was vanilla flavored. Round
slices having 60-cm2 surface areas were placed in sterile
petri plates. Surface contamination was eliminated by exposing the
cakes to UV light (three 6-W UV lights at 254 nm) during 30 min in a
Cleansphere CA100 unit by Safetech Limited (model F-0400; National
Labnet Co., Woodbridge, N.J.) under 85% RH (saturated KCl solution).
Inoculation of cakes.
Each of the five spore suspensions was
diluted to 103 CFU/ml, and they were mixed in equal
proportions. The inoculated cakes or petri plates were incubated at
21°C for up to 70 days. Four inoculation methods were examined.
(i) In the spot method (19), 10-µl spots of the spore
suspension were placed on the surface of a 60-cm2 slice of
cake having a thickness of approximately 1.5 cm. Growth was evaluated
by measuring the radial extension of the colonies.
(ii) In the spray method (
2,
4,
7), 200 µl of the spore
suspension was vaporized onto the cakes with a manual piston
atomizer
(IL-D Continental Industry, Oakville, Ontario, Canada).
The distance
between the spray nozzle and the cakes was maintained
at 15 cm. Growth
was evaluated by the time required to obtain
visible (1-mm-diameter)
colonies, as well as by the total number
of colonies.
(iii) In the talc method (
13), approximately 20 mg of
culture-containing talc was added to the 60-cm
2 surface of
the cakes. A sterile talc powder of calcium silicate
(Aldrich,
Milwaukee, Wis.) was mixed with an equal mass of the
spore suspension,
and the mixture was allowed to dry in a laminar
flow cabinet at 25°C
for 72 h. Following this drying step, the
talc powder was
estimated to contain 10
3 CFU/g by plating on acidified PDA.
The spore-containing talc
was added to the cake with the apparatus
shown in Fig.
1.
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FIG. 1.
Apparatus used for inoculation of sponge cakes with a
spore-containing talc powder. The handle of the hammer (A) is pulled to
a fixed level and released. The spring (B) propels the hammer head (C)
on the top of the 60-cm2 velvet support stand (D). A
portion of the talc found on the velvet fabric base (E), which had
previously been dipped in the mold-contaminated talc powder, then drops
onto the cake or petri dish to be inoculated. A detailed plan of the
design is available upon request.
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(iv) In the air cabinet method, a highly contaminated industrial
environment is simulated. Five PDA plates colonized by sporulating
mold
cultures (one petri plate for each strain) were opened in
a
0.53-m
3 cabinet equipped with a domestic fan. The cakes
were placed in
the cabinet for 3 min and then removed. To show that
this system
distributed the spores, petri plates containing PDA were
used
in one experiment instead of cakes.
The a
w of acidified PDA was probably greater than 0.99, but
the medium a
w was not adjusted at the various
a
w levels to which
the cakes were exposed. Rather, since
all five molds grew well
on this medium, the PDA plates served as a
control for total populations
in the samples.
Three plates or cakes were inoculated by each method, and three
independent replicates (different product lot) of each assay
were
carried out.
Humidity-controlled packaging.
The petri plates containing
the inoculated cake slices were placed in a 1.8-liter thermo-formed
polypropylene semirigid tray (model BQ180; InnovaPlast, Ville d'Anjou,
Quebec, Canada). The RH level inside the systems was controlled by
placing a thin layer of saturated solutions of NaCl or KCl in the
bottom of the tray to generate RHs of 75 and 85%, respectively. An
environment with 97% RH was achieved by adding pieces of water-soaked
cotton inside small aluminum dishes with the petri dishes. Four petri
dishes were placed in each tray. The trays were sealed with a Multipak 486 polyester-saran-polyethylene film with the following gas
transmission rates: H2O vapor transmission, 0.08 g/m2/24 h; 90% RH at 38°C; O2, 9 ml/m2/24 h at 75% RH; and CO2, 23 ml/m2/24 h at 75% RH. The sealed packages were stored at
(21 ± 1)°C for up to 70 days.
Analyses.
Viable spores in inoculum suspensions were
estimated by plating the suspensions on PDA and incubating the cultures
at 24°C for 5 to 7 days. The moisture content of the IMC was
determined by gravimetry; the samples were dried for 16 h at
70°C under a 25-inch vacuum, according to Association of Official
Analytical Chemists method 925.09 (5). An EEJA-3 unit
(Novasina, Zurich, Switzerland) enabled the determination of
aw levels of the IMC. RH levels in the containers were
verified with a Solomat MPM500e hygrometer equipped with a 355 RHX
probe (DurPro, Longueuil, Quebec, Canada).
The numbers and the diameters of the mold colonies were determined
without opening the container. No attempt was made to identify
the
species that were growing. Although this approach does not
enable the
study of individual species, the multiple-mold inoculum
was made in
order to reflect the phenomena that would occur under
commercial
conditions.
The pH of an aqueous slurry of 10 g of milled samples in 250 ml of
deionized water was measured on an expanded-scale Corning
140 pH meter.
The composition of the product was analyzed by standard
methods
(
5).
Desorption curves were established by placing the cakes in sealed
hermetic containers, to which saturated solutions generating
RH levels
of 0% (Drierite), 33% (magnesium chloride), 43% (potassium
carbonate), 59% (sodium bromide), 65% (sodium nitrite), 75% (sodium
chloride), 79% (ammonium chloride), or 85% (potassium chloride)
were
added. The system was incubated at 25°C for up to 20 days.
At various
times, samples were taken and analyzed for moisture
content.
Equilibrium was generally reached after 6 days of incubation.
| |
RESULTS |
Composition and physicochemical characteristics of the cakes.
The composition, aw, moisture content, and pH of the yellow
layer cakes are shown in Table 1. With
abundant nutrients (Table 1), basic pH, and an aw of 0.83, the cakes are good media for mold growth. Incorporation of 0.15%
potassium sorbate did not inhibit the sporadic mold growth on the
surfaces of cakes produced commercially. Since sorbate has little or no
activity at this high pH, these results are understandable. Cakes B and
C, containing cocoa powder, are apparently more susceptible to mold
growth, as white or grey colonies are more noticeable on dark surfaces of cake within 2 weeks of storage at 21°C.
The desorption isotherm curve of the cakes (Fig.
2) has a very steep slope with increasing
a
w beyond 0.60. This indicates
that at an a
w
above 0.60, the moisture content increases markedly
and that lowering
the moisture content and a
w as a means of controlling
microbial proliferation is not practical because of detrimental
organoleptic changes in the cakes.
Inoculation methods.
To assess the number of spores delivered
to the cake surface, plates containing acidified PDA were used as
targets for the various inoculation systems. This experiment also
served to determine the standard deviations of the methods. The highest
inoculation levels were achieved with the air cabinet method (Table
2). By the talc method, experimental
colony counts were in agreement with the inoculated populations (Table
2), despite our concern that lumps would occur and that CFU counts for
the plates would not reflect the mold population of the powder.
However, with the spray method, only a quarter of the expected
population was obtained. It was not determined if this was because some
droplets did not reach the plate or because droplets contained more
than one spore.
Random contamination by spores contained in a ventilated air cabinet is
an easy method of inoculation. However, this method
had the highest
standard deviation, 20% of the inoculation level
(Table
2). The talc
and spray methods were more consistent, as
13 and 11% variations,
respectively, were recorded. Although the
talc and spray methods used
in this study were more predictable
than the air cabinet system, care
had to be taken in standardization
of the various steps of the
inoculation techniques. With the talc
method, the critical points were
appropriate mixing of talc dust
and the spore suspension, pressure of
the velvet disk on the talc
powder, and distance of displacement of the
hammer. With the spray
method, the critical factors were distance
between the nozzle
and the cake and pressure applied on the spray
handle.
The growth curve obtained by the spot method was reproducible on PDA
petri plates (Fig.
3). The standard
deviations of the
colony surfaces varied between 5 and 17%, as a
function of incubation
time. Colonies were visible on PDA after 3 to 4 days of incubation
at 25°C. This method was the easiest to reproduce.
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FIG. 3.
Growth of a five-strain mixed mold population used to
inoculate cakes by the spot method at 97% (A), 85% (B), and 75% (C)
RH. As a control, growth on PDA at 97% RH is also shown (D).  , cake
A;  , cake B;  , cake C.
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|
The cake samples inoculated in the air cabinet and incubated at 97%
equilibrium RH (ERH) had colony counts 10 times lower
than those
obtained for PDA plates (Fig.
4). This
was not due
to an inadequacy of the cakes to support growth of the
molds,
since PDA counts were only slightly superior to those obtained
for the cakes by the talc and spray methods (Fig.
5 and
6).
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FIG. 4.
Growth of a five-strain mixed mold population used to
inoculate cakes by the air cabinet method at 97% (A), 85% (B), and
75% (C) RH. As a control, growth on PDA at 97% RH is also shown (D).
, cake A; , cake B; , cake C.
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FIG. 5.
Growth of a five-strain mixed mold population used to
inoculate cakes by the spray method at 97% (A), 85% (B), and 75% (C)
RH. As a control, growth on PDA at 97% RH is also shown (D). , cake
A; , cake B; , cake C.
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FIG. 6.
Growth of a five-strain mixed mold population used to
inoculate cakes by the talc method at 97% (A), 85% (B), and 75% (C)
RH. As a control, growth on PDA at 97% RH is also shown (D). , cake
A; , cake B; , cake C.
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|
Effect of relative humidity.
aw is the most
important factor determining whether a mold will grow and the rate at
which it will grow on intermediate-moisture foods (15). Mold
growth was much slower in the samples incubated in 75% RH, with all
inoculation methods (Fig. 3 to 6). With three inoculation methods
(spray, talc, and air cabinet), the rate of colony appearance and the
total number of colonies were affected by ERH. Colony counts for cakes
were similar in systems adjusted at 85 and 97% RH but lower for
samples incubated at 75% ERH (Fig. 4 to 6).
Shelf life.
A cake's shelf life ended when a mold colony
appeared. Regression analyses were performed using shelf life to
compare the effects of the inoculation methods. Correlation
coefficients (r2) of around 0.70 were
obtained between the spot method and the other methods of inoculation
(Fig. 7). The shelf lives of the talc,
air cabinet, and spray methods were much better correlated. As an
example, the shelf life data for the spray and talc methods showed an
r2 of 0.97. The spot inoculation method
was the easiest and most precise inoculation technique, but its shelf
life data differed slightly from those obtained by talc, spray, and air
cabinet inoculation.
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FIG. 7.
Regression analyses of shelf lives obtained for cakes
inoculated with a five-strain mixed mold suspension between the spot
method and the talc (), spray (), or air cabinet ( ) method.
r2 values were 0.68, 0.73, and 0.69, respectively.
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| |
DISCUSSION |
Misleading results can be obtained in mold-free shelf life studies
carried out with deliberate additions of spores to the surfaces of
products. The cultures used may not be representative of the ones in
the plant and may not develop well at the particular ERH level of the
product. Thus, as recommended by Seiler (15), we used a
mixture of five molds isolated from commercial products. Penicillium and Aspergillus are frequent spoilage
agents of cake (8, 12, 18), and Eurotium is
frequently recovered in studies of the shelf life of bakery products,
particularly in low-ERH environments (15). Thus, the
cultures used in this study (A. sydowii, A. ochraceus, P. funiculosum, and E. herbariorum) are representative of cake spoilage molds. The use of
a mixed culture instead of an individual culture provides a more
realistic estimate of the effects of ERH and cake composition on the
shelf lives of the cakes. However, with this approach, it is difficult
to determine which species is present on the moldy cake and whether the
experimental conditions alter the frequency of the strains that develop
on the cakes. Cake composition had a significant effect on mold
development, and this work obviously raises questions as to the effects
of pH, cocoa, and initial aw on the development of the
molds.
We expected that colonies would appear more quickly with the spot
inoculation method than with the other three methods, but this was not
the case. This confirms the data reported by Seiler (15), in
which differences in levels of mold contamination had a surprisingly
small effect on mold-free shelf life.
The cake samples inoculated in the air had colony counts 10 times lower
than those obtained for PDA plate controls. The reason for this
discrepancy is unknown. These results suggest that even with identical
exposures to air cabinet contaminations, the inoculation levels can
vary greatly as a function of the type of substrate exposed to the air.
The spot, spray, and talc methods are more reliable inoculation
techniques for studies involving different food matrices.
Treatment of the conidia, dry in talc or wet in spray, did not
influence the mold-free shelf life at 75 and 85% ERH. In these instances, the ERH was the determining factor in mold-free shelf life.
However, colonies appeared faster at 97% ERH with the spray method.
This suggests that mixing the spore suspension with talc may have
generated some form of stress on the conidia.
With the spray, talc, and air cabinet inoculation methods, the total
number of colonies and their appearance were affected by ERH. This
suggests that the conditions were selective for some mold strains. We
expected that A. sydowii, A. ochraceus, and
P. funiculosum would not grow as well at 75% ERH as
E. herbariorum. Of all these species, E. herbariorum has the lowest published minimal aw
(12).
The selection of a particular method will depend on the aims of the
study, the precision required, and the material constraints of the
laboratory. The easiest methods to carry out in this study were the
spot and air cabinet methods, but the air cabinet system suffers from
wide variations in inoculation levels. Although all four methods can be
used to evaluate the mold-free shelf life of cakes, the spot method was
the most appropriate for study of the effect of the environment on the
growth rate of the molds. Therefore, of the four methods tested, the
spot method appears to be the method of choice for most applications.
| |
ACKNOWLEDGMENTS |
We thank Carolyn Babcock from the Canadian Collection of Fungus
Cultures, Agriculture and Agri-Food, Ottawa, Canada, for the identification of the mold cultures and Marie-Claude Poiré and Culinar for technical and scientific support.
This work was supported by Culinar.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Food Research
and Development Center, Agriculture and Agri-Food Canada, 3600 Casavant Blvd., St.-Hyacinthe, Quebec, Canada J2S 8E3. Phone: (514) 773-1105. Fax: (514) 773-8461. E-mail: FUSTIERP{at}EM.AGR.CA.
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Appl Environ Microbiol, January 1998, p. 192-196, Vol. 64, No. 1
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
