PEER-REVIEWED ARTICLE bioresources.
com
Activity of Spent Coffee Ground Cinnamates against
Wood-decaying Fungi in vitro
Aitor Barbero-López,a,* Antonio Ochoa-Retamero,a Yeray López-Gómez,a Teemu
Vilppo,b Martti Venäläinen,c Anu Lavola,d Riitta Julkunen-Tiitto,d and Antti Haapala a,b
Fungi and microbes can remarkably degrade the appearance and
durability of organic materials, such as wood. The inhibitory effects of
natural phenolics may offer more sustainable alternatives to preserve
wood than the toxic biocides that are currently used. Although pure
caffeine has been proven to have antibacterial properties, the applicability
of spent coffee in wood preservation has not been determined. This work
conducted in vitro tests with three brown rot and one white rot fungi and
demonstrated the potential of spent coffee-derived cinnamates, analyzed
with high-performance liquid chromatography, as antimicrobial agents.
Spent coffee at concentrations of 1% and above in the growing media
caused significant growth suppression of all of the fungi. This was not only
because of the caffeine, but also the other chemicals present in the residue
extracts, which demonstrated that spent coffee could be used as a source
of green chemicals in wood preservative formulations.
Keywords: Biorefining; Preservatives; Secondary metabolites; Wood decay; Wood preservation
Contact information: a: School of Forest Sciences, University of Eastern Finland, FI-80101, Finland; b:
Department of Applied Physics, University of Eastern Finland, FI-70211, Finland; c: Natural Resources
Institute Finland, FI-58450 Punkaharju, Finland; d: Department of Environmental and Biological
Sciences, University of Eastern Finland, FI-80101, Finland;
* Corresponding author: [email protected]
INTRODUCTION
Increasingly strict legislation on toxic wood preservatives is driving the
development of green chemicals for wood. The use of many wood preservatives is limited
or banned, as chromated copper arsenate (Mohajerani et al. 2018). Other types of metal
salt, borate, and creosote products are still used, although constant pressure is applied by
the national chemicals agencies for less toxic substitutes. More limitations for wood
preservatives can be expected, as they belong to a class of so called emerging pollutants,
together with several pesticides and pharmaceuticals (Geissen et al. 2015).
Green chemicals that protect wood from decay and pathogens, while also
maintaining a low environmental impact (Ding et al. 2017), are sought from plant extracts.
Examples of these chemicals are the polyphenols, such as condensed tannins (Anttila et al.
2013) and stilbenes (Lu et al. 2016), known antifungals with some commercial products
already on the market. Novel and interesting sources for potential antifungals can be found
in industrial side-streams, such as coffee refining (Arora and Ohlan 1997; Acevedo et al.
2013). The phenolics and alkaloids (e.g. caffeine) in the side-streams of coffee refining
have no competing industrial use. Mazela et al. (2016) recently verified the antifungal
activity of purified caffeine in a wood preservation setting, while Lekounougou et al.
(2007) demonstrated its antifungal properties against some wood-decaying fungi.
Contradicting results have been found for bacteria; Sant’Anna et al. (2017) found that spent
Barbero-López et al. (2018). “Coffee grounds & fungi,” BioResources 13(3), 6555-6564. 6555
PEER-REVIEWED ARTICLE bioresources.com
coffee grounds (SCGs) does not inhibit the growth of different foodborne pathogenic
bacteria and phytopathogenic fungi, while Sousa et al. (2015) suppressed different disease-
causing bacteria and yeasts using spent coffee.
Despite several interesting functionalities of SCGs, the limited availability of the
raw material often renders their valorization economically unattractive. This has been
shown in the case of biodiesel production from SCGs (Kookos 2018), but obviously a
different outcome can be achieved if the end product has significantly higher market value
or lower cost of production. In most of the soluble coffee producing industries, the waste
is collected by specialized agencies, which sell the residues for different purposes (i.e.
composting, gardening, bioenergy production, mushroom growth) but for commercial or
household SCGs there is no established recovery and recycling system. Present studies
focus in different aspects of fresh and spent coffee. Their components have been
extensively analyzed (Mullen et al. 2013; Monente et al. 2015). Contemporary studies
concerning coffee have focused mostly on health implications (Koloverou et al. 2015), land
use, and climate issues (Ricketts et al. 2004). Studies on the revalorization of spent coffee
grounds have focused on energy applications (Santos et al. 2017) and food supplements
(Panzella et al. 2017). These studies and the recent reviews of this topic (Kourmentza et
al. 2018; Mata et al. 2018) do not address the potential of spent coffee-derived chemical
components as a potential resource for antifungal chemicals with applications, e.g. in wood
preservation.
In this paper we present for the first time the capacity of spent coffee as a green
alternative to reduce wood-decaying fungi growth. We also characterized fresh and spent
coffee grounds in terms of the chemical composition and assessed the efficiency of the
extracted chemical mixes against common wood-decaying fungi. Our aim was to determine
if the waste generated from coffee brewing has potential for use as a feedstock in chemical
extraction and if its functionality can be utilized in wood preservation or as an antifungal
in a more general context.
EXPERIMENTAL
Fresh and spent medium-roast coffee grounds (100% Coffea arabica) were tested
by extracting 50-g batches of coffee grounds in 1 L of boiling Milli-Q water (Merck KGaA,
Darmstadt, Germany) for 45 min to obtain a concentrated hot water extract with a low
number of volatile components. After extraction, the solids were removed with either a fine
sieve or 30-µm filter. The growth media included 4% malt powder and 2% agar, along with
1%, 2%, or 5% sieved spent coffee extracts (SCEs) (w/w), 1% filtered SCEs, or 1% fresh
coffee. Reference media were made with 1.6% copper-based preservative (Celcure C4,
Koppers Inc., Pittsburgh, PA, USA), 4% malt, and 2% agar to have an industrial NTR
(Nordiska Träskyddsrådet) AB-class standard capable preservative as reference. The
commercial copper-based wood preservative contained copper(II) carbonate (17%),
ethanolamine (< 35%), benzalkonium chloride (4.75%), cyproconazol (0.096%), sodium
nitrite (< 5%), and polyethoxylated tallow amine (< 5%).
The chemical composition of the SCEs was analyzed in detail with an HP 1100
Series LC-system (Agilent Technologies, Palo Alto, CA, USA) equipped with a diode array
detector, where the reverse-phase separation was performed on a Hypersil ODS (Thermo
Fisher Scientific, Waltham, MA, USA) with a RP C18 column (Thermo Fisher Scientific,
Waltham, MA, USA) with the dimensions 75 mm × 4.6 mm. Phenols were separated by
Barbero-López et al. (2018). “Coffee grounds & fungi,” BioResources 13(3), 6555-6564. 6556
PEER-REVIEWED ARTICLE bioresources.com
gradient elution using aqueous 1.5% tetrahydrofuran with 0.25% orthophosphoric acid (A)
and methanol (B) as eluents. The following elution gradient was used: 0 min to 5 min with
100% A, 5 min to 10 min with 85% A and 15% B, 10 min to 20 min with 70% A and 30%
B, 20 min to 60 min with 50% A and 50% B, and 60 min to 65 min with 100% B. The flow
rate was 2 mL/min, the column temperature was 30 °C, and the injection volume was 20
µL. The compounds were detected at a wavelength of 270 nm, and the tentative
identification was based on the retention time, UV spectra of the compounds, and the
literature. The quantification of the compounds was based on the response factors specific
to the standard compounds. Standards provided with the chemicals purchased from Sigma-
Aldrich (Sigma-Aldrich Finland Oy, Helsinki, Finland) were used in the identification and
quantification of the components in the coffee samples: chlorogenic acid for all of the
chlorogenic acid derivatives; ferulic acid; p-OH-cinnamic acid for the p-OH-cinnamic acid
derivatives; cinnamic acid for the caffeic acid derivatives; protocatechuic acid for the
protocatechuic acid derivative; and caffeine.
The growth reduction efficiency of the SCEs was tested in vitro with three brown
rot fungal strains (Coniophora puteana BAM 112, Gloeophyllum trabeum BAM 115, and
Rhodonia (Poria) placenta BAM 113) and a white rot fungal strain (Trametes versicolor
BAM 116) obtained from the Federal Institute for Materials Research and Testing (BAM,
Berlin, Germany). Fungal hyphae plug measuring 0.28 cm2 were placed in a petri dish (Ø
90 mm) and incubated with no light at 22 °C ± 2 °C and 70% relative humidity between 9
and 11 days, when the mycelium of the control fungi reached the edge of the dish. Between
six and ten replicates were prepared, depending on the species and its growth variability.
The growth rate inhibition was measured by following the method from Chang et al.
(1999). The inhibition rate of the fungal growth with the addition of extracts in the growth
media was assessed according to Eq. 1,
Inhibition (%) = (1 - (AT - IA) / (AC - IA)) × 100 (1)
where AT is the fungal area in the experimental sample (cm2), AC is the fungal area in the
control sample (cm2), and IA is the size of the inoculated plug (cm2). Pictures of the petri
dish were taken with the same set up as explained in Ancin-Murguzur et al. (2018).
The statistical significance of the coffee treatments was determined using Fisher’s
least significant difference test with the least significant difference as the post-hoc for the
analysis of variance using the software SPSS Statistics 23 (IBM, New York, USA).
RESULTS AND DISCUSSION
Most of the water-soluble, low molecular weight components, including sugars,
caffeine, and other polar compounds like phenolic compounds, were removed during the
first extraction (coffee brewing), which left less soluble components in the SCEs. Volatile
components and large molecular weight components, like tannins and carbohydrates, were
not detected. The amount of caffeine decreased significantly between the fresh coffee and
SCEs, and the concentrations of other components were also noticeably lower.
The phytochemical profiles (high performance liquid chromatography (HPLC)-
fingerprints) of the samples were comparable. Seventy and 75 different components above
the detection limit at 270 nm were separated from the SCEs made from fresh coffee and
the filtered fresh coffee sample, respectively. In the SCEs from the spent coffee grounds,
Barbero-López et al. (2018). “Coffee grounds & fungi,” BioResources 13(3), 6555-6564. 6557
PEER-REVIEWED ARTICLE bioresources.com
the number of components was consistent between the samples and was approximately half
of that in the fresh coffee samples (Table 1).
Table 1. Concentrations of the Compounds in Different Liquid Coffee Samples
Analyzed by HPLC
Filtered
Retention Fresh
Fresh SCEs Filtered SCEs
Compound Time Coffee
Coffee (mg/L) (mg/L)
(min) (mg/L)
(mg/L)
Protocatechuic acid der. 4.0 - - 2.7 2.1
Chlorogenic acid der. 1 4.1 39.3 33.6 - -
Chlorogenic acid der. 2 4.6 26.9 22.9 3.9 4.0
Chlorogenic acid der. 3 5.3 7.5 6.3 - -
Caffeine (alkaloid) 6.0 1104.1 934.3 31.7 31.0
Neochlorogenic acid 6.6 733.8 613.9 60.8 64.9
Chlorogenic acid der. 4 8.6 2.7 2.3 1.2 -
p-OH-Cinnamic acid der. 1 9.1 7.5 6.1 0.8 0.7
Chlorogenic acid der. 5 10.3 175.8 143.9 17.7 19.2
Chlorogenic acid 10.8 1138.7 949.6 97.9 102.3
Chlorogenic acid der. 6 11.5 638.7 526.1 58.2 58.2
p-OH-Cinnamic acid der. 2 13.3 5.0 4.9 0.6 -
p-OH-Cinnamic acid der. 3 13.6 7.5 5.0 0.5 0.3
Chlorogenic acid der. 7 14.0 18.6 14.9 0.8 0.8
Ferulic acid 14.4 120.1 99.1 11.4 11.4
Chlorogenic acid der. 8 15.3 67.6 56.0 7.2 8.9
Caffeic acid der. 1 16.7 1.4 1.4 - -
Caffeic acid der. 2 16.9 3.7 3.1 - -
Chlorogenic acid der. 9 18.6 4.3 3.0 - -
Chlorogenic acid der. 10 20.4 2.1 2.4 - -
Chlorogenic acid der. 11 20.6 1.5 1.8 - -
Chlorogenic acid der. 12 20.8 1.5 1.6 - -
Chlorogenic acid der. 13 21.3 4.2 1.8 1.0 0.7
Chlorogenic acid der. 14 21.7 7.4 3.3 0.6 0.9
Chlorogenic acid der. 15 22.2 76.3 59.5 18.7 19.2
Chlorogenic acid der. 16 22.6 49.1 36.4 9.2 9.8
Caffeic acid der. 3 24.9 1.5 1.0 0.4 0.3
Chlorogenic acid der. 17 25.2 9.6 7.9 2.0 2.2
Chlorogenic acid der. 18 25.9 72.8 58.0 13.8 15.7
Caffeic acid der. 4 28.4 1.0 1.0 0.1 0.2
Chlorogenic acid der. 19 29.5 9.6 8.9 1.4 2.0
Chlorogenic acid der. 20 32.5 4.1 4.7 - -
Total of cinnamates - 3240 2680 308 322
Barbero-López et al. (2018). “Coffee grounds & fungi,” BioResources 13(3), 6555-6564. 6558
PEER-REVIEWED ARTICLE bioresources.com
The coffee samples consisted of hydroxycinnamates, which were mainly different
derivatives of chlorogenic acid (caffeoylquinic acids) and ferulic acid, but also the
derivatives of caffeic and p-hydroxycinnamic acid. Additionally, one of the main
components in the samples was the methylxanthine alkaloid, caffeine.
Recently, Martínez et al. (2017) established that chlorogenic acid inhibits mycelial
growth and spore germination at doses of 15 μg/μL against phytopathogenic fungi relevant
in horticulture and agriculture. Chlorogenic acid has been known to be abundantly
available in industrial by-products, such as those derived from coffee (Murthy and Naidu
2012). The recovered phenolic components have mostly been considered for new value-
added products, such as phenolic antioxidant adjunct for food processing, but not for wood
preservation.
Caffeic and protocatechuic acids have been found to completely inhibit the growth
of two Aspergillus spp. molds at concentrations of 0.2 mg/mL and 0.3 mg/mL (Aziz et al.
1998). Cinnamic acid and its derivatives have been shown to inhibit the growth of Candida
albicans and A. niger at low doses (Narasimhan et al. 2004). Also, caffeic, chlorogenic,
ferulic, and trans-cinnamic acids have recently been reported to prevent the activity of
several Colletotrichum spp. isolates that cause anthracnose fruit rot (Roy et al. 2018).
The proportions of the compounds were similar between the two fresh coffee
samples and between the two SCEs samples. The compound amounts were highest in the
fresh coffee sample. Filtration of the fresh coffee reduced the concentrations of the
compounds, and thus the amount of cinnamic acids and caffeine in the filtered fresh coffee
sample was 17% and 15% lower, respectively, than in the unfiltered sample. In SCEs, the
difference in the total cinnamates between the filtered and unfiltered samples was
approximately 4%.
The SCEs inhibited the growth of the four species of decay fungi when applied at
concentrations of 1% and higher (Fig. 1). Arora and Ohlan (1997) concluded that 0.5%
caffeine fully inhibits fungal growth. The highest concentration (w/w) of SCEs in this study
was 5%, which indicated the presence of less than 0.1% caffeine. These findings agreed
with those of Arora and Ohlan (1997) but showed a stronger effect on G. trabeum compared
with pure caffeine. This indicated that there are synergistic effects between the chemicals
in spent coffee grounds that prevent the growth of wood-decaying fungi.
Filtering the SCEs caused a significant increase in the inhibition of C. puteana, G.
trabeum, and T. versicolor (see Fig. 2 for a practical example). Arora and Ohlan (1997)
found that filtering the coffee decreased its antifungal effect by 53%. This decrease in
effectiveness of the spent coffee when filtered may have been caused by the presence of
other chemicals, such as carbohydrates, that promote fungal growth and hinder the
antifungal activity of other chemicals.
A preliminary test was done based on the same method, but with 0.2% spent coffee
in the media. This test promoted the growth of G. trabeum (data not shown), which
supported the conclusion that there are chemicals present in the SCEs that promote the
growth of fungi. For C. puteana and R. placenta, the inhibition caused by 1% fresh coffee
did not differ significantly from that of the spent 5% SCEs. However, compared with the
other species, 1% fresh coffee caused the highest inhibition, which differed significantly
from that of the other concentrations. These differences indicated that chemicals present in
fresh coffee and not spent coffee can play a role in fungal inhibition. The medium with
1.6% copper-based preservative completely inhibited the growth of all of the fungi.
Barbero-López et al. (2018). “Coffee grounds & fungi,” BioResources 13(3), 6555-6564. 6559
PEER-REVIEWED ARTICLE bioresources.com
Fig. 1. Inhibition of wood-decaying fungi by fresh and spent coffee ground extracts: C. puteana,
G. trabeum, and R. placenta (N = 10), and T. versicolor (N = 6)
The statistical analysis confirmed that all the SCEs inhibited significantly
(P=0.000) the growth of all species of fungi when compared to reference media. Fresh
coffee caused a significantly higher inhibition than spent coffee in all fungi (P=0.000) and
filtering of 1% SCEs caused significant growth inhibition in all fungi (P<0.05) except R.
placenta when compared to 1% SCE.
Fig. 2. Growth of C. puteana (BAM 112) after 13 d in malt-agar media petri dish with the control
on the left and the 5% non-filtered spent coffee ground extract infused media on the right
During the experiment, a decolorized halo around the mycelia of C. puteana was
observed after 4 d to 5 d, which could have indicated that compounds were released by the
fungi that detoxified the growth media. This was similar to the results reported by Kovačec
et al. (2017).
Barbero-López et al. (2018). “Coffee grounds & fungi,” BioResources 13(3), 6555-6564. 6560
PEER-REVIEWED ARTICLE bioresources.com
The minimum inhibitory concentration (MIC) to completely inhibit the growth of
fungi was not determined, but the results showed that the MIC value was beyond 5% for
all of the fungi tested. This meant that spent coffee is not a feasible wood preservative, but
it could be considered a green source of chemicals that can contribute to preservative
formulations against fungi after selective separation and purification. Recent studies have
also found a high antioxidant activity in SCEs (Panusa et al. 2013) that is often related to
the natural durability of wood (Binbuga et al. 2008) and may enhance the potential for the
use of these extracts in wood preservative formulations.
The antifungal activity of the SCEs against wood-decaying fungi was thus because
of the caffeine, as well as several identified antifungal chemicals, such as chlorogenic acid
and ferulic acid derivatives and caffeic and p-hydroxycinnamic acids. These two sets of
chemicals suggested that there is a joint interaction with microbes and that those
components contribute to the decay resistance. Furthermore, previous studies have found
that low doses of some of the constituents of spent coffee inhibit different kinds of fungi
(Aziz et al. 1998; Narasimhan et al. 2004; Lekounougou et al. 2007). Alternative extraction
methods of spent coffee ground constituents, their selective separation, and further use in
wood preservative formulations may lead to novel methods for the use of bio-based
chemicals that can substitute current fungicides.
Recent investigations have presented spent coffee grounds as a useful substrate for
the cultivation of wood-degrading fungi that form edible mushrooms (Leifa et al. 2001).
In contrast, the findings in this paper showed that several extractives with antifungal
activities against wood-decaying fungi remain in coffee grounds after they are used for
making coffee. Fan et al. (2006) found that even if the fungus Pleurotus ostreatus still
fructified when grown with tannins and caffeine, increasing the concentrations of these
chemicals caused reductions in the mycelial growth of the fungus. Their study also found
that the tannins were completely degraded, while the caffeine was only partially degraded
and accumulated in the mycelium and fruiting bodies of P. ostreatus. Oh et al. (2018) found
that the mycelial growth of edible mushrooms decreased when coffee hydrolysates were
present in the media, but the antioxidant properties were improved and the number of
polyphenols of the mycelia increased. Extraction and selective removal of green chemicals
with an antifungal activity as a first step could lead to a better performance of the solid
fraction of spent coffee as a media for mushroom cultivation. For this application, both the
chemical recovery and mushroom cultivation need to be studied further.
Until recently, SCG has been discarded to landfills and considered solid waste with
low value. The commercial viability spent coffee ground chemicals will strongly depend
on availability of spent coffee grounds. The coffee industry generates large volumes of wet
SCGs from the manufacture of instant coffee and caffeinated drinks (Pfluger 1975), and
utilization of this resource is still a rather original and environmentally friendly approach
of international and societal interest, avoiding the disposal of such residue in landfills
(Stylianou et al. 2018). Collecting the waste from private users may not be a feasible option,
but collecting the SCGs from the coffee industry is a clear opportunity for its valorization.
CONCLUSIONS
1. We demonstrated that spent coffee ground extracts contain chemicals that inhibit the
growth of wood-decaying fungi at low concentrations. To extract and isolate antifungal
Barbero-López et al. (2018). “Coffee grounds & fungi,” BioResources 13(3), 6555-6564. 6561
PEER-REVIEWED ARTICLE bioresources.com
components from spent coffee grounds has high potential for developing green
preservatives and promoting the valorization of organic residues.
2. It was found that the antifungal activity was not solely derived from the presence of
caffeine, but also from the synergistic reactivity of the cinnamates and alkaloids that
were present in the residue at reasonable concentrations.
ACKNOWLEDGMENTS
This work was supported by the KAUTE Foundation and Teollisuusneuvos Heikki
Väänänen’s Fund.
REFERENCES CITED
Acevedo, F., Rubilar, M., Scheuermann, E., Cancino, B., Uquiche, E., Garcés, M.,
Inostroza, K., and Shene, C. (2013). “Spent coffee grounds as a renewable source of
bioactive compounds,” J. Biobased Mater. Biol. 7(3), 420-428.
DOI: 10.1166/jbmb.2013.1369
Ancin-Murguzur, F. J. Barbero-López, A., Kontunen-Soppela, S., and Haapala, A.
(2018). “Automated image analysis tool to measure microbial growth on solid
cultures”, Comput. Electron. Agric. 151, 426-430. DOI:
10.1016/j.compag.2018.06.031
Anttila, A.-K., Pirttilä, A. M., Häggman, H., Harju, A., Venäläinen, M., Haapala, A.,
Holmbom, B., and Julkunen-Tiitto, R. (2013). “Condensed conifer tannins as
antifungal agents in liquid culture,” Holzforschung 67(7), 825-832.
DOI: 10.1515/hf-2012-0154
Arora, D. S., and Ohlan, D. (1997). “In vitro studies on antifungal activity of tea
(Camellia sinensis) and coffee (Coffea arabica) against wood-rotting fungi,” J. Basic
Microb. 37(3), 159-165. DOI: 10.1002/jobm.3620370302
Aziz, N. H., Farag, S. E., Mousa, L. A. A., and Abo-Zaid, M. A. (1998). “Comparative
antibacterial and antifungal effects of some phenolic compounds,” Microbios.
93(374), 43-54.
Binbuga, N., Ruhs, C., Hasty, J. K., Henry, W. P., and Schultz, T. P. (2008). “Developing
environmentally benign and effective organic wood preservatives by understanding
the biocidal and non-biocidal properties of extractives in naturally durable
heartwood,” Holzforschung 62(3), 264-269. DOI: 10.1515/HF.2008.038
Chang, S.-T., Wang, S.-Y., Wu, C.-L., Su, Y.-C., and Kuo, Y.-H. (1999). “Antifungal
compounds in the ethyl acetate soluble fraction of the extractives of Taiwania
(Taiwania cryptomerioides Hayata) heartwood,” Holzforschung 53(5), 487-490.
DOI: 10.1515/HF.1999.080
Ding, T., Bianchi, S., Ganne-Chédeville, C., Kilpeläinen, P., Haapala, A., and Räty, T.
(2017). “Life cycle assessment of tannin extraction from spruce bark,” iForest 10(5),
807-814. DOI: 10.3832/ifor2342-010
Fan, L., Soccol, A. T., Pandey, A., de Souza Vandenberghe, L. P., and Soccol, C. R.
(2006). “Effect of caffeine and tannins on cultivation and fructification of Pleurotus
on coffee husks,” Braz. J. Microbiol. 37(4), 420-424.
Barbero-López et al. (2018). “Coffee grounds & fungi,” BioResources 13(3), 6555-6564. 6562
PEER-REVIEWED ARTICLE bioresources.com
DOI: 10.1590/S1517-83822006000400003
Geissen, V., Mol, H., Klumpp, E., Umlauf, G., Nadal, M., van der Ploeg, M., van de Zee,
S. E. A. T. M., and Ritsema, C. J. (2015). “Emerging pollutants in the environment: A
challenge for water resource management,” Int. Soil Water Conserv. Res. 3(1), 57-65.
DOI: 10.1016/j.iswcr.2015.03.002
Koloverou, E., Panagiotakos, D. B., Pitsavos, C., Chrysohoou, C., Georgousopoulou, E.
N., Laskaris, A., and Stefanadis, C. (2015). “The evaluation of inflammatory and
oxidative stress biomarkers on coffee–diabetes association: Results from the 10-year
follow-up of the ATTICA Study (2002–2012),” Eur. J. Clin. Nutr. 69(11), 1220-
1225. DOI: 10.1038/ejcn.2015.98
Kookos, I. K. (2018). “Technoeconomic and environmental assessment of a process for
biodiesel production from spent coffee grounds (SCGs),” Res. Con. Recyc, 134, 156-
164.
Kourmentza, C., Economou, C. N., Tsafrakidou, P., and Kornaros, M. (2018). “Spent
coffee grounds make much more than waste: Exploring recent advances and future
exploitation strategies for the valorization of an emerging food waste stream,” J.
Clean Prod. 172, 980-992. DOI: 10.1016/j.jclepro.2017.10.088
Kovačec, E., Regvar, M., van Elteren, J. T., Arčon, I., Papp, T., Makovec, D., and Vogel-
Mikuš, K. (2017). “Biotransformation of copper oxide nanoparticles by the
pathogenic fungus Botrytis cinerea,” Chemosphere 180, 178-185.
DOI: 10.1016/j.chemosphere.2017.04.022
Lekounougou, S., Ondo, J. P., Jacquot, J., Nevers, G., Gérardin, P., and Gelhaye, E.
(2007). “Effects of caffeine on growth of wood-decaying fungi,” in: The International
Research Group on Wood Protection, Stockholm, Sweden.
Leifa, F., Pandey, A. and Soccol, C. R. (2001). “Production of Flammulina velutipes on
coffee husk and coffee spent-ground,” Braz. Arch. Biol. Technol. 44, 205-212. DOI:
10.1590/S1516-89132001000200015
Lu, J., Venäläinen, M., Julkunen-Tiitto, R., and Harju, A. M. (2016). “Stilbene
impregnation retards brown-rot decay of Scots pine sapwood,” Holzforschung 70(3),
261-266. DOI: 10.1515/hf-2014-0251
Martínez, G., Regente, M., Jacobi, S., Del Rio, M., Pinedo, M., and de la Canal, L.
(2017). “Chlorogenic acid is a fungicide active against phytopathogenic fungi,”
Pestic. Biochem. Phys. 140, 30-35. DOI: 10.1016/j.pestbp.2017.05.012
Mata, T. M., Martins, A. A., and Caetano, N. S. (2018). “Bio-refinery approach for spent
coffee grounds valorization,” Bioresour. Technol. 247, 1077-1084.
DOI: 10.1016/j.biortech.2017.09.106
Mazela, B., Cofta, G., Perdoch, W., Gobakken, L. R., and Kwaśniewska-Sip, P. (2016).
“Decay resistance of wood treated with bio-friendly preservative systems,” in: 47th
IRG Annual Meeting, Lisbon, Portugal.
Mohajerani, A., Vajna, J., and Ellcock, R. (2018). “Chromated copper arsenate timber: A
review of products, leachate studies and recycling,” J. Clean Prod. 179, 292-307.
DOI: 10.1016/j.jclepro.2018.01.111
Monente, C., Ludwig, I. A., Irigoyen, A., De Peña, M.-P., and Cid, C. (2015).
“Assessment of total (free and bound) phenolic compounds in spent coffee extracts,”
J. Agr. Food Chem. 63(17), 4327-4334. DOI: 10.1021/acs.jafc.5b01619
Mullen, W., Nemzer, B., Stalmach, A., Ali, S., and Combet, E. (2013). “Polyphenolic and
hydroxycinnamate contents of whole coffee fruits from China, India, and Mexico,” J.
Agr. Food Chem. 61(22), 5298-5309. DOI: 10.1021/jf4003126
Barbero-López et al. (2018). “Coffee grounds & fungi,” BioResources 13(3), 6555-6564. 6563
PEER-REVIEWED ARTICLE bioresources.com
Murthy, P. S., and Naidu, M. M. (2012). “Recovery of phenolic antioxidants and
functional compounds from coffee industry by-products,” Food Bioprocess Tech.
5(3), 897-903. DOI: 10.1007/s11947-010-0363-z
Narasimhan, B., Belsare, D., Pharande, D., Mourya, V., and Dhake, A. (2004). “Esters,
amides and substituted derivatives of cinnamic acid: Synthesis, antimicrobial activity
and QSAR investigations,” Eur. J. Med. Chem. 39(10), 827-834.
DOI: 10.1016/j.ejmech.2004.06.013
Oh, N.-S., Sung, N.-Y., Byun, E.-H., Kim, Y.-E., Cho, E.-J., and Oh, C.-H. (2018).
“Changes in mycelial growth and antioxidant activities of basidiomycetous strains
added with hydrolysates of spent coffee grounds as a substrate,” J. Korean Soc. Food
Sci. Nutr. 47(1), 90-95. DOI: 10.3746/jkfn.2018.47.1.090
Panusa, A., Zuorro, A., Lavecchia, R., Marrosu, G., and Petrucci, R. (2013). “Recovery
of natural antioxidants from spent coffee grounds,” J. Agr. Food Chem. 61(17), 4162-
4168. DOI: 10.1021/jf4005719
Panzella, L., Pérez-Burillo, S., Pastoriza, S., Martín, M. Á., Cerruti, P., Goya, L., Ramos,
S., Rufián-Henares, J. A., Napolitano, A., and d’Ischia, M. (2017). “High antioxidant
action and prebiotic activity of hydrolyzed spent coffee grounds (HSCG) in a
simulated digestion-fermentation model: Toward the development of a novel food
supplement,” J. Agr. Food Chem. 65(31), 6452-6459. DOI: 10.1021/acs.jafc.7b02302
Pfluger, R. A. (1975). “Soluble coffee processing,” in: Solid wastes: origin, collection,
processing, and disposal, C. L. Mantell (ed.), New York: Wiley.
Ricketts, T. H., Daily, G. C., Ehrlich, P. R., and Michener, C. D. (2004). “Economic
value of tropical forest to coffee production,” P. Natl. Acad. Sci. USA 101(34),
12579-12582. DOI: 10.1073/pnas.0405147101
Roy, S., Nuckles, E., and Archbold, D. D. (2018). “Effects of phenolic compounds on
growth of Colletotrichum spp. in vitro,” Curr. Microbiol. 75(5), 550-556.
DOI: 10.1007/s00284-017-1415-7
Sant’Anna, V., Biondo, E., Kolchinski, E. M., da Silva, L. F. S., Corrêa, A. P. F., Bach,
E., and Brandelli, A. (2017). “Total polyphenols, antioxidant, antimicrobial and
allelopathic activities of spend coffee ground aqueous extract,” Waste Biomass
Valori. 8(2), 439-442. DOI: 10.1007/s12649-016-9575-4
Santos, C., Fonseca, J., Aires, A., Coutinho, J., and Trindade, H. (2017). “Effect of
different rates of spent coffee grounds (SCG) on composting process, gaseous
emissions and quality of end-product,” Waste Manage. 59, 37-47.
DOI: 10.1016/j.wasman.2016.10.020
Sousa, C., Gabriel, C., Cerqueira, F., Manso, M. C., and Vinha, A. F. (2015). “Coffee
industrial waste as a natural source of bioactive compounds with antibacterial and
antifungal activities,” in: The Battle Against Microbial Pathogens: Basic Science,
Technological Advances and Educational Programs, A. Méndez-Vilas (ed.),
Formatex Research Center, Badajoz, Spain, pp. 131-136.
Stylianou, M., Agapiou, A., Omirou, M., Vyrides, I., Ioannides, I. M., Maratheftis, G.,
and Fasoula, D. (2018). “Converting environmental risks to benefits by using spent
coffee grounds (SCG) as a valuable resource,” Environ Sci Pollut Res, 1-15. DOI:
10.1007/s11356-018-2359-6
Article submitted: April 20, 2018; Peer review completed: June 28, 2018; Revised
version received and accepted: July 9, 2018; Published: July 11, 2018.
DOI: 10.15376/biores.13.3.6555-6564
Barbero-López et al. (2018). “Coffee grounds & fungi,” BioResources 13(3), 6555-6564. 6564