Prevalence of spoilage mold in coffee before and after brewing

Abstract

Commercial ground coffee must be safe for consumption and comply with the regulation applied in a country. However, the risk of the occurrence of spoilage molds in commercial ground coffee, particularly toxigenic mold originated from coffee cherries or green beans, is still a major concern of the coffee industry. This study evaluated the prevalence of spoilage mold in fifteen brands of commercial ground coffee. The spoilage molds were also determined after traditional brewing (non-filtration brewing). The mold counts were enumerated on dichloran-glycerol 18% agar by spread plate method. The spoilage molds were also morphologically identified after isolation on malt extract agar and potato dextrose agar. The results showed that low numbers of molds were found in all samples before brewing, in a range of 10 to 200 CFU/g. A total of eleven genera were identified. Aspergillus, Cladosporium and Penicillium were found as the predominating genera. After brewing, molds from genera Alternaria and Aspergillus were still found. However, the total counts decreased to the level between undetected to an average of 3 CFU/mL. This study highlighted that very low levels of spoilage mold was recovered after brewing which may not pose a health risk.

Full text

*Corresponding author.
Email: h_kusumaningrum@ipb.ac.id
eISSN: 2550-2166 / © 2019 The Authors. Published by Rynnye Lyan Resources
Food Research 3 (6) : 720 - 726 (December 2019)
Journal homepage: http://www.myfoodresearch.com
FULL PAPER
Prevalence of spoilage mold in coffee before and after brewing
*Kusumaningrum, H.D. and Rasyidah, M.M.
Department of Food Science and Technology, Faculty of Agricultural Technology, Bogor Agricultural
University, Bogor 16680 Indonesia
Article history:
Received: 4 April 2019
Received in revised form: 25
May 2019
Accepted: 28 May 2019
Available Online: 11 June
2019
Keywords:
Commercial ground coffee,
Mold counts,
Spoilage mold,
Traditional brewing
DOI:
https://doi.org/10.26656/fr.2017.3(6).142
Abstract
Commercial ground coffee must be safe for consumption and comply with the regulation
applied in a country. However, the risk of the occurrence of spoilage molds in commercial
ground coffee, particularly toxigenic mold originated from coffee cherries or green beans,
is still a major concern of the coffee industry. This study evaluated the prevalence of
spoilage mold in fifteen brands of commercial ground coffee. The spoilage molds were
also determined after traditional brewing (non-filtration brewing). The mold counts were
enumerated on dichloran-glycerol 18% agar by spread plate method. The spoilage molds
were also morphologically identified after isolation on malt extract agar and potato
dextrose agar. The results showed that low numbers of molds were found in all samples
before brewing, in a range of 10 to 200 CFU/g. A total of eleven genera were identified.
Aspergillus, Cladosporium and Penicillium were found as the predominating genera. After
brewing, molds from genera Alternaria and Aspergillus were still found. However, the
total counts decreased to the level between undetected to an average of 3 CFU/mL. This
study highlighted that very low levels of spoilage mold was recovered after brewing which
may not pose a health risk.
1. Introduction
The quality of green coffee beans can affect the
characteristic of coffee beverages and is still a major
concern in the coffee industry worldwide. Once the
green beans are contaminated, it can decrease the quality
and sensory characteristics of the roasted and brewed
coffee, giving the unwanted attributes (Iamanaka et al.,
2014). The presence of filamentous molds has been
already reported in coffee beans processed in Brazil,
Malaysia, Philippines, Thailand, and Saudi Arabia (Silva
et al., 2008; Noonim et al., 2008; Alvindia and Acda,
2010; Rahim et al., 2011; Al-Abdalall and Al-Talib,
2012). Aspergillus, Penicillium, Fusarium and
Cladosporium have been found as natural coffee
contaminants in Brazil (Silva et al., 2008) and present in
coffee beans from the field, during fermentation and
drying to the warehouse. Alvindia and Acda (2010) also
reported that fourteen genera were recovered from coffee
beans in the Philippines after harvest and drying. The
mold contamination can occur on coffee beans as a result
of improper harvesting procedures, inappropriate drying,
and inadequate storage conditions. The diversity of the
contaminant molds can also be influenced by the region
where the coffee beans originated (Noonim et al., 2008;
Couto et al., 2014).
Although the roasting temperature of coffee beans
can eliminate the contaminant mold, however, some
spores are not completely eliminated and would be
carried over in coffee products. Rahim et al. (2011)
reported that molds of different genera were still found
on eight of twenty commercial black coffee powder
samples in Malaysia. Fusarium sp. dominated the
contamination, followed by Penicillium sp., Aspergillus
sp., and Cladosporium spp. Alvindia and Acda (2010)
also reported that nine species from five genera were
recovered from 21 samples of roasted coffee bean from
retail markets in Philippines. Aspergillus, Penicillium,
Chrysosporium, Microascus and Rhizopus were found as
coffee contaminants.
Usually, coffee is consumed after hot brewing
preparation using a coffee machine or a coffee maker,
where filtering is included (Verst et al., 2018). However,
despite different modern coffee brewing techniques are
available, the traditional brewing process is still popular
in Indonesia (Sudiyarto et al., 2012). This type of coffee
known as ‘kopi tubruk’ or mud coffee in Indonesia is
prepared by putting the ground coffee in a cup followed
by pouring hot water and held for a few minutes before

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serving to let the residues settle down.
Although concerns on the presence of spoilage
molds in coffee have been increasing, data on the
presence of carried over mold in coffee after brewing
have not been widely reported. This study was carried
out to determine the presence of mold in coffee before
brewing and molds that survive after brewing.
2. Materials and methods
2.1 Samples
A total of fifteen commercial ground coffee samples
were purchased from the supermarket around Bogor,
Indonesia. The samples consisted of Robusta, Arabica,
and a mix of Arabica-Robusta ground coffee. For each
sample, a sample size of 100 g was collected and
subsampled (25 g) for determination of the mold counts.
From the 100 g of laboratory sample, 10 g of the
sample was also weighed and brewed in 150 mL hot
water (90oC) without filtering, representing the
traditional practice to prepare mud coffee. This mixture
was agitated with a spoon for approximately 10 s and
then placed at room temperature for 4 mins to settle the
residue, prior to the mold determination. For pH
measurement, the brewed coffee was further cooled until
reaching the room temperature (27± 1°C).
2.2 Enumeration of mold counts
A total of 25 g of ground coffee was aseptically
mixed with 225 mL 0.1% buffered peptone water
(Oxoid, UK) in a sterile stomacher bag and homogenized
in a stomacher (BagMixer 400P, Interscience, France)
for 2 mins to provide the first suspension. For brewed
coffee after cooled, the first dilution was made by adding
of 25 mL beverage solution aseptically to 225 mL 0.1%
peptone water and homogenized. Serial dilutions were
made under aseptic conditions. For each dilution, 0.1 mL
was then pipetted and spread on duplicate plates of
solidified dichloran 18% glycerol agar (DG-18, LabM,
UK). Plates were incubated at 25oC for 5 days and the
colonies were counted and expressed as CFU/g. All
samples were analyzed twice.
2.3 pH measurement
The pH of ground coffee was measured using the
first suspension, while the pH of the brewed coffee was
measured after the coffee was cooled to room
temperature.
2.4 Isolation and identification of mold
Any visible mycelia growth or spores from DG-18
plates were transferred onto malt extract agar (MEA,
Merck, Germany) and potato dextrose agar (PDA,
Oxoid, UK) plates for identification. The plates were
incubated at 25oC for 7 days. Isolates were identified on
the basis of macro-morphological properties of colonies
and micro-morphological properties of conidia and other
structures by referring to the key described by Pitt and
Hocking (2009).
3. Results and discussion
3.1 Molds counts in coffee before and after brewing
The total molds in commercial ground coffee before
brewing were found in a range between 10 CFU/g to 200
CFU/g (Table 1). These loads decreased after brewing,
between undetected level (no colony) to an average of 3
CFU/mL. The pH was in a range of 5.12 to 6.12 before
brewing and slightly decreased after brewing to between
5.04 to 5.88. The fact that low numbers of mold were
still found after brewing in some coffee samples
indicated that the spores of some molds were likely
resistant to heat treatment during brewing.
The mold counts found in ground coffee before
brewing in this study were comparable with the study
conducted by Alvindia and Acda (2010) and by Rahim et
al. (2011). Alvindia and Acda (2010) reported that total
mold in roasted bean coffee in Philippines was in a range
of 5.3 x 101 to 1.4 x 102 CFU/g. Rahim et al. (2011)
reported that commercial black coffee powder samples in
Malaysia were contaminated by mold in a range of <100
to 1.2 x 103 CFU/g. The presence of mold in roasted
ground coffee was influenced by the place of origin of
the coffee beans and the processing methods involved.
After roasting, the total mold in coffee beans decreased
significantly by 93 to 97% (Alvindia and Acda, 2010).
The presence of mold after roasting might be due to the
post-processing contaminations, the heat resistance of
mold spores, or associated with insufficient heat
treatment during roasting.
3.2 Mold isolates from coffee before brewing
As shown in Table 2 and 4, more than 250 mold
colonies were found on plates from coffee samples
before and after brewing. Some molds with similar
morphology were found on some plates. From those
colonies, sixty isolates were discovered. Some isolates
were not identified. Eleven genera were identified on
samples before brewing, i.e. Cladosporium, Penicillium,
Aspergillus, Alternaria, Geothricum, Phoma, Rhizopus,
Chrysonilia, Curvularia, Pestalotiopsis and Fusarium
(Table 2). Morphological appearance and growth of
some isolates on PDA and MEA plates are presented in
Table 3.
The genera Aspergillus, Penicillium, Cladosporium,
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and Fusarium were also detected in commercial black
coffee powder samples in Malaysia (Rahim et al., 2011).
The presence of environmental molds in commercial
ground coffee, particularly Aspergillus, Penicillium, and
Fusarium is of the most concern because these molds are
known to produce harmful mycotoxins to human.
Aspergillus flavus was detected in three samples of
commercial ground coffee in this study. The presence of
A. flavus in coffee beans has been reported by Alvindia
and Acda (2010) after harvest, drying, and on roasted
beans from retail markets. A. flavus has also been
detected on green coffee during fermentation, drying,
and storage in polystyrene and jute sacks (Silva et al.,
2008). However, the presence of toxigenic mold in
coffee does not always indicate the presence of
mycotoxins, since many factors influence the
FULL PAPER
No. Sample Code Type of Coffee Mold counts (log CFU/g) pH
Before brewing After brewing Before brewing After brewing
1 KP1 Robusta-Arabica 1.2±0.3a NC 5.80±0.00 5.55±0.01
2 KP2 Robusta 1.5±0.2 a NC 6.12±0.01 5.78±0.08
3 KP3 Robusta 1.4±0.6 a 0.3 ± 0.4 6.05±0.01 5.88±0.01
4 KP4 Robusta-Arabica 1.0±0.0 a NC 5.99±0.01 5.73±0.01
5 KP5 Robusta 1.3±0.4 a NC 6.03±0.01 5.34±0.01
6 KP6 Robusta 1.2±0.0 a NC 5.54±0.00 5.26±0.01
7 KP7 Robusta-Arabica 1.0±0.0 a 0.5 ± 0.7 5.46±0.00 5.22±0.01
8 KP8 Robusta 2.3±0.2b 0.5 ± 0.2 5.63±0.00 5.38±0.00
9 KP9 Robusta 1.5±0.8ab 0.2 ± 0.2 5.86±0.01 5.57±0.01
10 KP10 Robusta 1.5±0.3 a NC 5.36±0.01 5.30±0.01
11 KP11 Robusta 2.0±0.5 ab 0.3 ± 0.0 5.53±0.01 5.43±0.00
12 KP12 Arabica 1.3±0.4 a 0.1 ± 0.1 5.36±0.00 5.17±0.00
13 KP13 Robusta 2.2±0.6 ab 0.2 ± 0.2 5.40±0.00 5.17±0.00
14 KP14 Robusta 2.2±0.1 b NC 5.59±0.00 5.20±0.00
15 KP15 Arabica 2.2±0.0 b NC 5.12±0.00 5.04±0.00
Table 1. Mold counts and pH of commercial ground coffee and brewed coffee.
NC = no colonies found
Genera Species Isolate Frequency Coffee samples
Alternaria Alternaria sp. (1) 12 19 KP 3, 6, 8, 9,10, 12
Alternaria sp. (2) 27 3 KP 6, 8
Aspergillus Aspergillus flavus 41 57 KP 10, 11, 12
Aspergillus niger 57 3 KP 10, 14
Cladosporium Cladosporium cladosporioides 15 24 KP 2, 4, 5, 8
Cladosporium sp. (1) 16 35 KP 5, 8, 10, 13, 14, 15
Cladosporium sp. (2) 18 2 KP 5, 14
Cladosporium sp. (3) 24 22 KP 5, 9, 14, 15
Cladosporium sp. (4) 28 2 KP 7
Chrysonilia Chrysonilia sp. 6 15 KP 2, 11, 12, 15
Curvularia Curvularia lunata 44 6 KP 6, 14
Curvularia pallesence 45 3 KP 10, 14
Fusarium Fusarium sp. 53 1 KP 15
Geotrichum Geotrichum sp. (1) 1 19 KP 1, 2, 3, 14
Geotrichum sp. (2) 4 4 KP 1, 9
Pestalotiopsis Pastalotiopsis sp. 21 2 KP 5
Penicillium Penicillium citrinum 51 3 KP 15
Penicillium corylophilum 50 2 KP 15
Penicillium islandicum 31 3 KP 8
Penicillium sp. (1) 17 2 KP 5
Penicillium sp. (2) 30 4 KP 8, 15
Penicillium sp. (3) 34 3 KP 9, 14
Penicillium sp. (4) 48 2 KP14
Penicillium sp. (5) 49 20 KP 9, 10, 12, 14, 15
Phoma Phoma sp. 13 2 KP 3, 11
Rhizopus Rhizopus sp. 40 2 KP 5, 11
Table 2. Identified mold from commercial ground coffee before brewing

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biosynthesis of mycotoxin. Production of mycotoxin
such as aflatoxin is depending on environment condition,
particularly water activity and temperature (Mannaa and
Kim, 2017).
Furthermore, molds belonging to genera Fusarium,
Pestalotia, Paecelomyces and Penicillium were also
detected in coffee cherries, whereas Fusarium,
Penicillium as well as Aspergillus were also found in
dried coffee beans (Silva et al., 2008). Djossou et al.
(2015) also reported that Aspergillus niger, Aspergillus
fumigati, Penicillium, Fusarium, and Mucor
contaminated coffee beans from Ivory Coast. Alvindia
and Acda (2010) reported that molds from different
genera were found in roasted beans, such as Aspergillus
chevalieri, Aspergillus flavus, A. niger, A. fumigatus,
Chrysosporium spp., Microascus spp., Penicillium
citrinum, Penicillium janczewskii, and Rhizopus oryzae.
Furthermore, Al-Abdalall and Al-Talib (2012) also
reported the occurrence of filamentous mold in coffee
beans (Coffea arabica L.) from grocery stores and retail
markets in an eastern region of the Kingdom of Saudi
Arabia. The predominating genera were Aspergillus,
with the highest frequency found was A. niger (74.71%).
Several molds from other genera were also isolated such
as Fusarium solani (3.56%), A. flavus (2.01%), and
Penicillium oxalicum (1.61%).
FULL PAPER
Morphology on Microscopy Genera
(Sample) PDA-above PDA-bottom MEA-above MEA-bottom
Alternaria
(KP3.4)
Aspergillus
(KP12.3)
Cladosporium
(KP4)
Curvularia
(KP12.2)
Fusarium
(KP15.4)
Geothricum
(KP1.1)
Penicillium
(KP 11.4)
Pestalotiopsis
(KP5.6)
Table 3. Macroscopic and microscopic appearance of mold isolates after 7 days of incubation at 25°C

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As shown in Table 2, Cladosporium was found as
the most often detected on the coffee samples before
brewing, i.e. it was found in 10 of 15 samples.
Cladosporium was also found in commercial black
coffee powder samples in Malaysia, although in a lower
frequency than Fusarium (Rahim et al., 2011).
Cladosporium is known as the most abundant fungi in
outdoor and indoor air (Bensch et al., 2018). The
conidium Cladosporium is adaptable in the air because it
is small, dry, lightweight, and resistant to sunlight (Pitt
and Hocking, 2009). Silva et al. (2008) reported that
Cladosporium was detected in coffee cherries collected
from trees, during fermentation and was still found after
drying and during storage of dried coffee beans.
In this study, although in low counts, mold from
genera Alternaria was found in six of ten coffee samples.
Alternaria alternata (1.2%) was also reported by Al-
Abdalall and Al-Talib (2012) in coffee beans from
different grocery stores and retail markets. Alternaria
species are generally found as saprophytes and
endophytes of a wide range of plants pre- and post-
harvest (Woudenberg et al., 2013; Lee et al., 2015).
Several taxa, however, were also found as important
postharvest pathogens and airborne allergens
(Woudenberg et al., 2013). In another study, A. alternata
together with Cladosporium cladosporioides,
Pestalotiopsis sp., Phoma exigua var. exigua and Phoma
herbarum, as endophytic fungi, were also isolated from
leaves of Coffea arabica L. in Brazil (Fernandes et al.,
2009). The author also pointed out that antibacterial,
fungicidal and herbicidal activities were showed by a
high proportion of endophytic mold. The culture of A.
alternate was found as potential antibacterial and
antifungal source.
The other molds that were identified in this study
were from genera Chrysonilia, Pestalotiopsis and
Phoma. The species C. sitophila formerly was known as
Monilia sitophila (Pitt and Hocking, 2009). The genus
Chrysonilia includes three species, i.e. C. sitophila, C.
crassa and C. tetrasperma. Chrysonilia sitophila has
been reported as an inducer of occupational asthma cases
in person involved in the coffee industry (Francuz et al.,
2010). Pestalotiopsis isolates were obtained from leaves
of Coffea arabica in Southern China (Song et al., 2013).
Pestalotiopsis species is known as weak plant pathogens,
but also as common endophytes produces bioactive
compounds. Phoma is a soil mold that can attack the
coffee leaves and cherries. Couto et al. (2014) reported
that Phoma was also found on coffee beans under
organic and conventional cultivation. Other genera were
also found such as Aspergillus, Penicillium, Fusarium,
Cladosporium, Mucor, Rhizopus, Trichoderma,
Colleototrichum, Epicoccum, Bipolaris, Glomerella,
Colletotricum, Gliocladium and Alternaria. Organic
coffee beans demonstrated greater mold diversity than
conventional coffee beans.
3.3. Mold isolates from brewed coffee
Some molds were recovered after the coffee was
brewed in hot water at 90oC (Table 4). Some molds were
not identified. However, the total molds in brewed
coffees decreased to a low level or undetected as
presented in Table 1. The temperature applied for coffee
brewing in this study was higher than that found in the
study of Verst et al. (2018). Verst et al. (2018) studied
the dispensing and serving temperatures of coffee-based
hot beverages in the home and in the food service
industry. The study reported that of 356 coffees in the
food service industry and 110 coffees in private
households, the dispensing temperatures were in a range
of 58–86°C with an average at 75±5°C.
As presented in Table 4, Alternaria sp. (isolate 12
and 27) were found in five samples, whereas Aspergillus
sp. (isolate 54 and 55) were found in two samples of
brewed coffee. The presence of Alternaria sp. in brewed
coffee, indicated that they likely produced spores that
could be regarded as heat resistant. Ascospore-forming
Aspergillus, together with Byssochlamys, Talaromyces,
and Penicillium were reported by Pitt and Hocking
(2009) belong to the most commonly occurring heat-
resistant molds.
In general, the pasteurization process at temperature
of 70oC for 10 mins can inactivate Aspergillus,
Fusarium, Penicillium, Mucor and Rhizopus (Yaguchi et
al., 2012). However, Jesenská et al. (1993) reported that
A. fumigatus, Aspergillus nidulans, Eupenicillium
baarnense and Ulocladium spp. were still recovered after
heat treatment at 80°C for 60 mins. The survival of
Acremonium sclerotigenum, A. ochraceus,
Botryotrichum piluliferum, Byssochlamys fulva,
Gilmaniella humicola, Neosartorya fischeri,
FULL PAPER
Sample
Code Type of Coffee Isolate Genera
KP3 Robusta 2,3,11, 14 Not identified
12 Alternaria sp. (1)
KP7 Robusta-Arabica 55 Aspergillus sp. (2)
KP8 Robusta
3, 11, 14, 39 Not identified
12, Alternaria sp. (1)
27 Alternaria sp. (2)
54 Aspergillus sp. (1)
KP9 Robusta 2, 3, 14, 39 Not identified
12 Alternaria sp. (1)
KP11 Robusta 3 Unidentified
KP12 Arabica 12 Alternaria sp. (1)
14 Not identified
KP13 Robusta 39 Not identified
Table 4. Identified mold from brewed coffee

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Nodulisporium sp. and Talaromyces avellaneus was even
still found after heating at 90°C for 10 mins.
Furthermore, the heat resistance of molds from
genus Aspergillus which were isolated from spoiled
pasteurized product has been reported by Berni et al.
(2017). The D values in glucose solution of Aspergillus
hiratsukae (≡Neosartorya hiratsukae), A. neoglaber
(≡Neosartorya glabra), and A. thermomutatus
(≡Neosartorya pseudofischeri) were in a range between
3.7 to 13.5 mins at 87°C; 1.5 to 3.5 mins at 90°C; and
0.3 to 0.4 mins at 95°C.
4. Conclusion
This study showed that a low level of mold was
found in commercial ground coffee before brewing, in a
range of 10 to 200 CFU/g. Cladosporium, Aspergillus
and Penicillium were recovered as prevalent and
important genera before brewing. However, the brewing
process reduced the mold counts and the diversity of the
mycobiota. Aspergillus sp. and Alternaria sp. were still
recovered in very low numbers that expected did not
appear to pose a health risk. This study also highlighted
that the quality and safety of commercial coffee should
be regularly monitored, to obtain and/or maintain safe
coffee products for the consumers. Investigating the
mycoflora of commercial coffee before and after
brewing is worthwhile in providing an overview of the
safety of coffee products for consumption.
Conflict of Interest
The authors declared no potential conflict of interest
related to the article.
Acknowledgments
The authors thank Ir. Ina Retnowati at
Phytopathology Laboratory of SEAMEO BIOTROP
Indonesia for her valuable help and technical assistance
during identification of mold isolates. The authors also
thank the Department of Food Science and Technology,
Faculty of Agricultural and Technology, Bogor
Agricultural University for facilitating this research.
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