High power ultrasonics as a novel tool offering new opportunities for managing wine microbiology

Abstract

Industrial scale food and beverage processes that utilize microorganisms are typically faced with issues related to the exclusion, suppression or elimination of spoilage organisms. Yet the use of traditional anti-microbial treatments such as heat, chemical biocides or sterile filtration may themselves be restricted by regulations or else be undesirable due to their adverse sensory impacts on the product. High power ultrasound (HPU) is a technology whose application has been evaluated if not exploited in several food and beverage processes but has yet to be introduced into the wine industry. This review examines the research findings from related industries and highlights possible applications and likely benefits of the use of HPU in winemaking.

Full text

REVIEW
High power ultrasonics as a novel tool offering new
opportunities for managing wine microbiology
Vladimir Jiranek Æ Paul Grbin Æ Andrew Yap Æ
Mark Barnes Æ Darren Bates
Received: 24 May 2007 / Revised: 18 August 2007 / Accepted: 18 August 2007
Ó Springer Science+Business Media B.V. 2007
Abstract Industrial scale food and beverage pro-
cesses that utilize microorganisms are typically faced
with issues related to the exclusion, suppression or
elimination of spoilage organisms. Yet the use of
traditional anti-microbial treatments such as heat,
chemical biocides or sterile filtration may themselves
be restricted by regulations or else be undesirable due
to their adverse sensory impacts on the product. High
power ultrasound (HPU) is a technology whose
application has been evaluated if not exploited in
several food and beverage processes but has yet to be
introduced into the wine industry. This review
examines the research findings from related industries
and highlights possible applications and likely ben-
efits of the use of HPU in winemaking.
Keywords Fermentation management 
High power ultrasound  Spoilage 
Wine
Introduction
Electrical energy can be converted into ultrasonic
sound waves (20 kHz–10 MHz), which are above the
range of human hearing (16–20 kHz). The applica-
tions of such outputs depend on the sound intensity
and its frequency. While many are familiar with the
exploitation of diagnostic ultrasound (1–10 MHz) in
medicine, the use of power (20–100 kHz) and high
frequency (100 kHz–1 MHz) ultrasound are less well
recognized. Of particular interest here is high power
ultrasound (HPU), which typically utilizes sound
intensities above 1 W/cm
2
and frequencies in the
power ultrasound range (McClements 1995; Leighton
1998; Villamiel and de Jong 2000b). When radiated
into a liquid or slurry, HPU achieves both chemical
and physical effects. This occurs through the forma-
tion and collapse (cavitation) of high-energy micro-
bubbles (Maisonhaute et al. 2002; Krefting et al.
2004; Leighton 2007). The conditions within these
collapsing bubbles generate localized temperatures
exceeding 5500°C and pressures of up to 50 MPa
(Leighton 1998). The shock waves that are released
from the collapse of the unstable bubbles transfer
kinetic energy, acoustic streaming that transfers heat
and mass, and vibration. The high-shear energy wave
V. Jiranek (&)  P. Grbin
School of Agriculture, The University of Adelaide, Food
and Wine, PMB 1, Glen Osmond, Adelaide, SA 5064,
Australia
e-mail: vladimir.jiranek@adelaide.edu.au
A. Yap  D. Bates
Cavitus Pty Ltd, P.O. Box 260, Crafers, Adelaide, SA
5152, Australia
M. Barnes
Applied Centre for Structural and Synchrotron Studies,
University of South Australia, Mawson Lakes Campus,
Adelaide, SA 5095, Australia
D. Bates
Innovative Ultrasonics Pty. Ltd, Noosa, QLD 4567,
Australia
123
Biotechnol Lett
DOI 10.1007/s10529-007-9518-z

can travel at some 570 km/h at the surface of solid
boundaries.
The applications for HPU in food processing are
numerous (e.g., see review by Knorr et al. 2004) and
include degassing, extractions, induction of oxida-
tion/reduction reactions, enzyme inactivation and
nucleation for crystallization processes, cleaning of
organic/inorganic surfaces and porous interior struc-
tures, reducing the particle size and variability in
liquid suspensions, and the defouling of filters. HPU
has not been applied to wine-making but offers
potential applications in several areas of the wine-
making process, Effects of HPU on microbes are
briefly reviewed below before some key opportunities
for the use of HPU technology in modulating
microbial activity and load at various stages of
winemaking in juice, musts, wines and barrels are
discussed.
Effects on microorganisms
While ultrasound below the cavitational threshold has
been used to enhance microbial productivity in
various bioreactor systems (Chisti 2003), cavitation
through HPU is generally associated with the killing
of microbial cells (Piyasena et al. 2003). Such killing
has been observed for bacteria, yeast, fungi, algae and
protozoa (Table 1).
The kinetics of microbial inactivation are first
order or pseudo first order (Furuta et al. 2004;
Tsukamoto et al. 2004; Zhang et al. 2006) with
Table 1 Microorgansims inactivated by ultrasound irradiation
Organism Matrix Reference
Bacteria
a
Legionella pneumophila
Gr+
Diluted medium Dadjour et al. (2006)
Escherchia coli
Gr-
Milk, juices Zenker et al. (2003)
Escherchia coli
Gr-
Saline Duckhouse et al. (2004)
Escherchia coli
Gr-
Water Furuta et al. (2004)
Faecal coliforms
Gr-
and streptococci
Gr+
Municipal wastewater Blume and Nies (2003)
Lactobacillus acidophilus
Gr+
Milk, juices Zenker et al. (2003)
Bacillus subtilis
Gr+
Nutrient broth Joyce et al. (2003)
Salmonella Senftenberg 775W
Gr-
McIlvaine citrate-phosphate
buffer or nutrient broth
A
´
lvarez et al. (2006)
Pseudomonas flourescens
Gr-
TSB medium Villamiel and de Jong (2000a)
Streptococcus thermophilus
Gr+
TSB medium Villamiel and de Jong (2000a)
Yeast
Saccharomyces cerevisiae Water Borthwick et al. (2005); Lo
¨
rincz (2004);
Tsukamoto et al. (2004)
Saccharomyces cerevisiae Sabouraud growth medium Guerrero et al. (2001)
Dekkera bruxellensis Saline Yap et al. (2007b)
Unspecified Orange juice Valero et al. (2007)
Fungi
Aspergillus flavus
b
Sabouraud growth medium Lo
´
pez-Malo et al. (2005).
Penicillium digitatum
b
Sabouraud growth medium Lo
´
pez-Malo et al. (2005).
Unspecified Orange juice Valero et al. (2007).
Algae
Microcystis aeruginosa BG11 growth medium Zhang et al. (2006).
Protozoa
Cryptosporidium parvaum Water Tsukamoto et al. (2004).
a
Gram positive or negative status indicated by the appropriate superscript after the species name
b
Experiments performed with spores
Biotechnol Lett
123

disinfection varying according to the power (Guerrero
et al. 2001; Furuta et al. 2004; Tsukamoto et al.
2004) and frequency (Borthwick et al. 2005). Tsu-
kamoto et al. (2004) showed that the rate of
inactivation of Saccharomyces cerevisiae yeast cells
by ultrasonic irradiation was a function of the
amplitude of the ultrasonic wave and the initial cell
numbers and was highest at higher amplitudes and
lower initial cell numbers. Subsequently, Borthwick
et al. (2005) reported that yeast cell disruption was
greater in a novel compact 267 kHz sonicator than in
a lower frequency 20 kHz probe sonicator at the same
exposure time.
The application of ultrasound together with ano-
ther disinfection technique such as antibiotics
(Peterson and Pitt 2000), heat (e.g. Villamiel and de
Jong 2000a; Lo
´
pez-Malo et al. 2005;A
´
lvarez et al.
2006), hypochlorite (Duckhouse et al. 2004), pres-
sure (Piyasena et al. 2003), TiO
2
photocatalyst
(Dadjour et al. 2006) or UV irradiation (Blume and
Neis 2004) has been reported to have synergistic
effects compared with each modality on their own.
Low frequency ultrasound rendered Escherichia coli
in biofilms more susceptible to gentamicin. Such
enhancement increased with increasing ultrasonic
intensity and decreased with increasing frequency
(Peterson and Pitt 2000). Similarly, low frequency
ultrasound (20 kHz) resulted in greater reductions in
the viability of Aspergillus flavus and Penicillium
digitatum spores when applied simultaneously with
heat (45–60°C) compared with either treatment alone
(Lo
´
pez-Malo et al. 2005). In the context of wine
production, it is unlikely that the co-application of
antibiotics, hypochlorite, pressure and TiO
2
will be
possible from a practical or legislative point of view.
Moreover, chemical additives work against the image
of wine as a ‘natural’ product. By comparison, heat as
a co-treatment with HPU may warrant further
investigation.
Generally a winemaker seeks to avoid higher
temperatures because of the adverse effect they have
on the flavour profile and colour of wine (Boulton
et al. 1996). For this reason, the heating of wine to
augment the effects of HPU would not be a preferred
option for winemakers. However, other points in the
production process are routinely exposed to heat, e.g.
the washing of fermentation tanks and barrels with
hot water. In this latter setting, and as discussed
below, considerable benefits associated with the
introduction of HPU could be expected. Thus rather
than merely use high pressure hot water to sanitize a
barrel or fermentation vessel, hot water together with
HPU may prove either i) more effective, ii) allow
lower temperature water to be used with the same
effectiveness or iii) permit the application of HPU for
a reduced period of time.
Possible applications of HPU to wine microbiology
Winemaking can be a constant struggle to suppress or
minimize the influence of undesirable microorgan-
isms at essentially all stages of the process. As a
result, there are many opportunities during the
conversion of grapes to finished wine at which a
technology such as HPU could be applied (Table 2).
Table 2 Opportunities for manipulating the microbiology of winemaking using HPU technology
Processing Stage/Substrate Treatment objective/outcome
Grapes or must from unsound fruit held in or being
transferred (by pumping) to fermentation vessels.
Reduction in load of spoilage organisms, enhanced extraction
of colour and flavour compounds into the juice/wine.
Fermenting must, completed fermentations or stuck
fermentations in tank or barrels.
Reduction of contaminating organisms (yeast or bacteria) prior to:
–inoculation with rescue yeast
–initiation of the malolactic fermentation (MLF).
Suppression or delay of MLF.
Acceleration of autolysis to encourage MLF.
Cleaning of barrels and tanks. Elimination of tartrate deposits and deep-seated microbial
contamination of oak.
Rejuvenation of oak.
Biotechnol Lett
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Amelioration of juice or must
Fruit can carry unacceptably large loads of spoilage
organisms, particularly where it is damaged or
overripe (reviewed by Amerine and Kunkee 1968;
Louriero and Malfeito-Ferreira 2003; Ribereau-Ga-
yon et al. 2000, Fugelsang and Edwards 2007).
These organisms include yeasts such as unwanted
Saccharomyces or Kloeckera, Hanseniaspora, Mets-
chnikowia, Candida, Pichia and Zygosaccharomyces
as well as the Gram-positive lactic acid and Gram-
negative acetic acid bacteria. If left unchecked, such
organisms can have a marked influence on the
ability of the desired or inoculated organism to
become established in primary or secondary fer-
mentation, and are likely to have a negative impact
on the final composition and sensory properties of
the wine (Sponholz 1993). The possibility of
applying HPU to inactivate such organisms before
the primary fermentation is quite attractive. The
most convenient means for applying HPU might be
by way of a flow-through system (Chisti 2003)
during juice or must transfer. A side-benefit of such
a system when used with musts (i.e., crushed grapes,
including solids) could be the enhancement of
colour and flavour extraction (A.Yap, pers. comm.).
In some circumstances, the direct application of
HPU to the juice or must in a tank, might also be
feasible.
Control of spoilage or inoculated microorganisms
during fermentation
Even with sound grapes, spoilage organisms can
build to problematic numbers during the primary or
secondary fermentation. Strategies for dealing with
contaminated fermentations depend on the nature,
timing and extent of the contamination. During the
primary fermentation, spoilage organisms most com-
monly develop in the latter stages especially where
the fermentation has become stuck (Boulton et al.
1996; Fugelsang and Edwards 2007). When it is yeast
that has an unacceptably large presence, an inocula-
tion with an appropriately conditioned ‘rescue yeast’
is often made. The aim of this action is to ensure the
numerical dominance of the desired strain and to
facilitate the rapid completion of the fermentation. In
more severe cases the fermentation may require
clarification by chilling, settling and then filtration
before being re-inoculated. Filtration is also used in
cases of bacterial spoilage, particularly where cor-
rection (reduction) of the pH of the wine, increased
sulfur dioxide concentrations or the addition of
lysozyme are ineffective or incompatible with the
intended wine processing and style. Such clarification
is itself seen as undesirable by some winemakers who
feel filtration imparts unwanted effects on the flavour,
colour or mouthfeel of the wine. Filtration is also not
appropriate in red winemaking during fermentation,
as limits skin contact.
HPU therefore represents a promising alterna-
tive for the reduction or elimination of unwanted
microbes during primary fermentation. Application
could conceivably be achieved via a flow-through
system during transfer of juice or musts from tank to
tank, or else by way of direct treatment of a tank or
barrel of juice or wine. Importantly, such effects are
expected to be achievable without the need for further
additives or time-consuming clarification of the wine.
Analogous opportunities for HPU can be envisaged in
the secondary or malolactic fermentation (MLF).
Mediated by lactic acid bacteria, the MLF results in
the decarboxylation of malic acid to lactic acid with
an associated decrease in acidity, reduced risk of
microbial spoilage via nutrient depletion and flavour
complexity of the wine (Laurent et al. 1994; Liu
2002). MLF is applied almost routinely to red wines
for stability, particularly by producers in the New
World, whereas application to white wines is more
restricted and occurs primarily for deacidification or
flavour effects. In either case there are instances
where the winemaker seeks to stop MLF, either
because an indigenous, non-preferred strain is dom-
inating or the spontaneous MLF is unwanted.
The delay or suppression of MLF may well be
readily achieved by HPU irradiation of the wine after
primary fermentation. Benefits of this technology
would be that no additives or filtration steps are
needed. In addition, where wines are held in oak
barrels, their treatment would also be possible in situ,
as the sound emitter (i.e., the sonotrode) can be
introduced through the barrel bung hole thereby
obviating the need for transfer of the wine to an open
tank (Yap et al. 2007a). Conversely, HPU might be
used to stimulate MLF through the provision of
nutrients. It is clear that many strains of Oenococcus
oeni, the primary MLF bacterium, have fastidious
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123

growth requirements (Garvie 1967; Edwards and
Fugelsang 2007). Therefore, HPU treatment of wines
post primary fermentation has the potential to not
only reduce microbial cell numbers prior to MLF but
also liberate the essential growth factors and nutrients
such as amino acids as these cells are disrupted.
A further opportunity for benefiting from HPU
relates to those wines being aged sur lee, that is, on
the sediment of yeast cells used in the primary
fermentation (Boulton et al. 1996; Ribe
´
reau-Gayon
et al. 2006). Such an aging technique is often used
with Chardonnay-based wines held in barrels and is
carried out with the aim of imparting greater flavour
and mouthfeel complexity to the wine (Iland and
Gago 2002). The means by which these sensory
changes occur is through the autolysis of the yeast
and thereby release of cellular enzymes and macro-
molecules into the wine (reviewed by Charpentier
and Feuillat 1993; Feuillat 2003). By increasing the
rate and extent of yeast cell disruption, HPU is
expected to offer benefits similar to other novel
means (e.g. Todd et al. 2000) of increasing yeast
autolysis. As stated, HPU has the additional advan-
tage of being readily applied to wines in barrels (Yap
et al. 2007a) and not requiring other changes to
winemaking practices.
Barrel sanitization
Barrels made of oak wood and used for the matura-
tion of wine or even the conduct of fermentation are
intrinsically difficult to clean. Washes performed
between fills usually only remove lees and loose
deposits: tartrate deposits remain, as would any
microbes entrapped therein. Certainly, the barrels
are not sterilized. This fact partly explains the growth
in the incidence of Dekkera/Brettanomyces spoilage
problems around the globe. This organism is most
commonly encountered in barrel-aged wines of
higher pH (i.e., *4) and low sulphur dioxide content.
It is able to develop from low cell numbers found in
contaminated barrels and produce sensory conse-
quences such as the generation of unpleasant odour
compounds, particularly 4-ethylphenol (Fugelsang
et al. 1993; Snowdon et al. 2006). As yet, there is
no convenient method for decontaminating barrels.
Steam treatment of barrels can kill Dekkera/Bretta-
nomyces cells in oak wood but only to a depth of
2 mm (Malfeito-Ferreira et al. 2004). Microbes
found deeper in the wood where the wine has
penetrated (i.e. up to 8 mm) were unaffected.
Regarding the decontamination of wine, sterile
filtration currently appears to be the only option,
and the barrels remain unusable. Preliminary data
from our laboratory clearly shows high rates of
inactivation of suspensions of active cultures of
Dekkera/Brettanomyces bruxellensis using HPU (Yap
et al. 2007b). Kill rates of [97% were observed even
after exposure times of only 90–120 sec at 50 watts.
While only laboratory based assays using freshly
grown yeast cultures have been obtained, comparable
results for actual wines in barrel using appropriately
scaled-up hardware and power densities are antici-
pated. Moreover, the application of HPU directly to
contaminated wines in barrels is expected to target
cells that are located deep within the pores of the
wood, which would otherwise be unaffected by
existing barrels treatments.
Conclusions
Findings from related areas of research strongly
suggest that HPU will yield benefits for the wine
industry. Even when considering only the use of HPU
to disrupt and inactivate microbial cells, potential
areas of application extend across the winemaking
process. It is therefore expected that this promise will
drive current and future work to fully the define the
application protocols and full extent of the impact of
HPU to winemaking. Furthermore, applications
beyond the management of wine microbiology will
no doubt also come to light.
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