Food Bioprocess Technol (2014) 7:1–20

DOI 10.1007/s11947-013-1168-7

REVIEW

Biological Aspects in Food Preservation by Ultraviolet

Light: a Review
Elisa Gayán & Santiago Condón & Ignacio Álvarez

Received: 15 February 2013 / Accepted: 29 July 2013 / Published online: 17 August 2013
# Springer Science+Business Media New York 2013

Abstract The potential to commercialize nonthermal ultravi- CPD Cyclobutan pyrimidine dimer
olet (UV) light technologies as new methods for preserving DewPP Dewar valence isomers
food products has caught the attention of a food industry that DSB Double-strand break
wishes to fulfill consumers' demands for fresh products. HS Heat shock
Numerous investigations have demonstrated UV light's ability HSP Heat shock proteins
to inactivate a wide range of microorganisms. However, the IR Infrared radiation
lack of UV sensitivity data from pathogenic and spoilage LHR Liquid holding recovery
bacteria is evident. In addition, the main factors associated LP Low-pressure mercury vapor lamps
with UV light in terms of microbial lethality remain unclear. MM Minimal medium
This review surveys critical factors (process, microbial, and MP Medium-pressure mercury vapor lamps
environmental parameters) that determine UV microbial resis- NER Nucleotide excision repair
tance and assess the effects of such factors on the inactivation ppGpp Guanosine 5′-diphosphate 3′-diphosphate
mechanism and repair pathway efficiency. The effects of some PRR Post-replication repair
of these factors, such as prior sublethal stresses and post- PUV Pulsed UV lamp
recovery conditions of UV treatments, may extensively im- PX Pulsed xenon lamp
prove the damage repair capacity and thus microbial surviv- RAMER RecA-mediated excision repair
ability. Further research is needed to establish adequate control ROS Reactive oxygen species
measures pre- and post-UV treatments. Furthermore, the pos- SP Spore photoproduct
sibility of combining UV light with conventional preservatives SSB Single-strand break
and other nonthermal technologies was assessed. The combi- TLS Translesion DNA synthesis
nation of UV light with mild heating or oxidant compounds
could offer promising treatments to enhance the safety and
stability of minimally processed foods.

Keywords UV light . Bacteria inactivation . DNA repair . Introduction

Sub-lethal stress . Combined processes
Traditionally, ultraviolet (UV) light irradiation has been used
Abbreviations as a disinfectant for air, surface, and water decontamination.
6-4PP Pyrimidine 6–4 pyrimidone photoproduct Recently, the food industry has shown increasing interest in
8-oxodGuo 8-Oxo-7,8-dihydro-2′-deoxyguanosine using UV irradiation for the hygienization of liquid foods and
AOP Advanced oxidation processes the surfaces of solid foods. As an emerging nonthermal pro-
BER Base excision repair cessing technology, UV irradiation offers multiple advantages:
effective inactivation of a broad range of spoilage and patho-
genic microorganisms, minimal loss of the nutritional and
E. Gayán : S. Condón : I. Álvarez (*)
sensorial quality of foods, no known toxic effects or residues
Tecnología de los Alimentos, Facultad de Veterinaria, Universidad de
Zaragoza, C/ Miguel Servet 177, CP 50013 Zaragoza, Spain from the treatment, and low energy consumption compared to
e-mail: ialvalan@unizar.es other thermal and nonthermal pasteurization processes.
2 Food Bioprocess Technol (2014) 7:1–20
UV light refers to the part of the electromagnetic spectrum
which ranges from 200 to 400 nm, and it is divided into three
regions: short-wave ultraviolet (UV-C), from 200 to 280 nm;
UV-medium wave (UV-B), from 280 to 320 nm; and UV-long
wave (UV-A), from 320 to 400 nm. The effects of UV light on
genetic material are primarily responsible for microbial inac-
tivation, although other cellular components such as proteins
can be also damaged. UV-C constitutes the most germicidal
region, and the peak of maximum effectiveness is at wave-
lengths of about 260–265 nm, corresponding with the peak of
maximum DNA absorption (Fig. 1) (Kowalski 2009). UV-C
absorption induces the formation of DNA photoproducts, in
particular cyclobutane pyrimidine dimers and pyrimidine 6–4
pyrimidone photoproducts, which inhibit transcription and
replication and eventually lead to mutagenesis and cell death.
Since UV-related microbial inactivation arises primarily
from the effects of UV light on genetic material, the UV
resistance of a specific microorganism depends on the effec-
tiveness of its DNA repair mechanisms as well as the extent of
DNA damage induced by the treatment (López-Malo and
Palou 2005). In addition, DNA damage and repair mecha-
nisms are affected by different factors, classified as microbial,
environmental, and processing factors, which can act before,
during, or after UV treatments.
For instance, bacteria change their physiology under differ-
ent growing conditions (growth medium, incubation tempera-
ture, and growth rate), which could vary their UV resistance
significantly (López-Malo and Palou 2005). Stress history
prior to UV treatment, such as heat, acid, osmotic, and starva-
tion shocks, may also influence resistance by triggering co-
protective adaptation responses (Van der Veen and Abee
2011). Recovery conditions also affect cell viability after irra-
diation, especially the exposure to visible light and growth or
recovery medium composition (Ganesan and Smith 1968;
Sommer et al. 2000). Temperature increments during treatment
and the addition of prooxidant chemical compounds may
improve UV lethality (Koivunen Heinonen-Tanski 2005;
Fig. 1 Comparisons of the relative germicidal efficiency of UV wave-
lengths, comparing LP (1), MP (2), and PX lamps (3) with germicidal
effectiveness for E. coli (dotted line)
Gayán et al. 2011). Consequently, as UV light technology
gains interest as a strategy for food decontamination, the
impact of these factors on microbial UV resistance must be
well understood in order to assess the actual lethality implica-
tions of UV light.
Thus, the objective of this review is to compile up-to-date
knowledge about the influence of process, microbial, and
environmental factors that could affect UV treatments for
bacteria and bacterial spores. This review will evaluate the
influence of these factors on UV survivability and lethality on
the basis of inactivation and damage repair. To achieve this
goal, the review will first describe the general mechanisms of
inactivation and repair. Based on those, the influence of the
lethality and survivability factors will be discussed.
Mechanisms of Inactivation by UV Radiation
Genetic materials are the primary targets of UV radiation, and
the types of lesions produced depend on the radiation band
(UV-C, UV-B, or UV-A). UV-C induces the formation of
photoproducts due to the direct absorption of photons by
pyrimidine and purine nucleic acid bases (López-Malo and
Palou 2005). Although both pyrimidine and purine bases are
strong UV-C photon absorbers, pyrimidines absorb about 10
times more than purines. Therefore, photoproducts derived
from pyrimidines are the most important (Kowalski 2009).
The major lesions induced by UV-C are cyclobutane pyrimi-
dine dimers (CPDs) and pyrimidine 6–4 pyrimidone photo-
products (6-4PPs) (Friedberg et al. 2006).
CPDs are formed when there are two adjacent pyrimidines
and a photon being absorbed by one pyrimidine. Pyrimidines
become covalently linked when the saturation of the carbon
atoms (C) 5 and 6 of both neighboring bases causes the
formation of a ring structure (Fig. 2(a)). CPDs are formed
between thymines (TT), cytosines (CC), or cytosine and thy-
mine (CT or TC) bases, depending on nucleotide composition.
In general, dimers containing thymines are most likely to
occur (Rastogi et al. 2010).
A similar process creates 6-4PPs, except that adducts are
generated by cycling between the C5–C6 bond of a pyrimi-
dine and the C4 carbonyl or imino groups (for thymine or
cytosine, respectively) for its 3′ neighbor. The resulting
oxetane and azetidine products are unstable and rapidly
rearrange themselves, transferring the carbonyl or amino
group of the 3′ base to the C5 position of the 5′ base, yielding
the 6-4PP (Fig. 2(c)). In this case, 6-4PPs are more frequently
observed with CC and TC, while TT or CT sequences are less
common. When exposed to UV-A or UV-B, 6-4PP can be
converted into Dewar valence isomers (DewPPs). However,
this damage is less common (Rastogi et al. 2010).
The proportion of 6-4PPs is much lower than that of CPDs,
accounting for about 25 % of total UV-mediated DNA
Food Bioprocess Technol (2014) 7:1–20
Fig. 2 Primary DNA photoproducts caused by UV-C and UV-B: cyclobutan pyrimidine dimer (CPD) (a), spore photoproduct (SP) (b), pyrimidine 6–4
pyrimidone photoproduct (6-4PP) (c), and 8-oxo-7,8-dihydro-2′-deoxyguanosine (8-oxodGuo) (d)
damage (Sinha and Hader 2002). This is probably because the
efficiency of the dimerization process, given by the quantum
yield (Φ), is higher for CPDs (Φ254 nm =22–26) than for 6-
4PPs (Φ254 nm =1.4) (Görner 1994). However, 6-4PPs are
potentially more lethal and mutagenic than CPDs because of
lower repair efficiency (Koehler et al. 1996). Both CPDs and
6-4PPs cause structural distortions in DNA molecules that
interfere with normal RNA transcription and DNA replication,
leading to mutagenesis and ultimately to cell death (Friedberg
et al. 2006).
Bacterial spores are also affected when they are exposed to
UV-C light. Spore photoproducts (SPs) are the major DNA
lesions in UV-irradiated bacterial spores (Douki et al. 2005;
Moeller et al. 2007). SPs are formed by the addition of a
methyl group of thymine residue to the C5 position of an
adjacent thymine (5-thyminyl-5,6-dihydrothymine, Fig. 2(b))
(Rastogi et al. 2010). SP formation is related to the dehydrated
A-conformation of the DNA molecule. Hence, SPs have also
been isolated in vegetative cells at low relative humidity
(Peccia et al. 2001). The consequences of SPs are similar to
those indicated for CPDs and 6-4PPs.
CPDs and 6-4PPs are also produced by bacterial spores, but
in very small quantities compared to SPs (Douki et al. 2005;
Moeller et al. 2007). For instance, Douki et al. (2005) reported
that the CPD yield induced by UV-C in Bacillus subtilis spores
was only 0.1 % that of SPs, and the levels for 6-4PPs were
even lower. This could be attributed to the fact that the quan-
tum efficiency for SP formation by 254 nm radiation (252
3
lesions per 104 per J/cm2) is higher than for the generation of
other photoproducts (1.0 CPD and 0.1 6-4PP per 104 per J/
cm2) (Setlow 2006). However, SPs are much less lethal than
CPDs or 6-4PPs, as SPs can be repaired efficiently in the first
minutes of spore germination via different mechanisms
(Setlow 2006). This could also explain the higher UV-C resis-
tance of bacterial spores compared to their corresponding
vegetative cells (Setlow 2001), since the quantum yield for
SP formation in bacterial spores is similar to that for CPD and
6-4PP in growing cells (Setlow 2006). Single- and double-
strand breaks (SSBs and DSBs) can be also detected at high
UV fluence to a small extent. Slieman and Nicholson (2000)
applied a UV-C dose of 16 kJ/m2 to dried B. subtilis spores.
Whereas nearly 40 % of the total chromosomal thymine was
converted within the SPs, only 0.3 and 0.16 % were present in
the SSBs and CPDs, respectively. Thus, CPDs, SSBs, and
DSBs probably do not have major physiological consequences
for the UV-C survival of spores (Slieman and Nicholson 2000).
When cells are exposed to UV-B radiation, fewer CPDs, 6-
4PPs, and DewPPs are produced compared to those in UV-C
radiation (Ravanat et al. 2001; Pattison and Davies 2006). Other
photoproducts may occur to a smaller extent, such as cytosine
photohydration, guanine bases oxidations, or adduct formation
between either two adjacent adenine bases or between adenine
and vicinal thymine (reviewed in Ravanat et al. 2001).
UV-A radiation produces less photochemical damage be-
cause of DNA's low absorbability in this range. CPDs are
formed about 105-fold less efficiently than at 254 nm, and 6-
4 Food Bioprocess Technol (2014) 7:1–20
4PPs are barely detectable. On the other hand, DewPPs are
induced more frequently here than by UV-B (Girard et al.
2011). DNA photooxidation damage of pyrimidine and purine
bases is also produced by UV-A. Guanine is the base most
susceptible to oxidization, resulting in 8-oxo-7,8-dihydro-2′-
deoxyguanosine (8-oxodGuo, Fig. 2(d)), the most frequently
seen oxidative lesion under UV-A radiation (Douki et al.
2003). Oxidation-damaged bases result in nonbulky lesions
that exert fewer obstacles for replication and transcription,
leading to DNA mutagenesis and the production of mutant
proteins (transcriptional mutagenesis). In addition, UV-A ra-
diation can also produce SSBs, but in very low numbers.
Overall, despite the low energy of UV-A photons for pyrim-
idine dimer formation, CPDs represent the main source of
DNA damage, followed by purine oxidations (essentially 8-
oxoG), pyrimidine oxidations, and SSBs in a ratio of 10:3:1:1
(Douki et al. 2003).
Finally, besides DNA damage, UV-A photooxidation af-
fects other biological targets such as proteins, lipids, and
sterols. In fact, proteins are major cellular targets for photo-
oxidation due to both their high abundance and the presence
of endogenous chromophores within their structures (certain
amino acid side chains, as well as bound chromophores such
as flavins and porphyrins). Direct damage induced by UV-A
radiation is limited to a small number of amino acid residues,
mainly tryptophan (Trp), tyrosine (Tyr), histidine (His), and
disulfide (cystine). However, most UV-induced protein dam-
age occurs indirectly, mediated by reactive oxygen species
(ROS) which react preferentially with Trp, His, Tyr, methio-
nine (Met), cysteine (Cys), and cystine side chain residues.
When these residues are initially altered, multiple secondary
processes occur, resulting in damage to other intra- and
intermolecular sites. These processes can lead to protein frag-
mentation, aggregation, and altered physical and chemical
properties, resulting in the loss of functionality (reviewed in
Pattison and Davies 2006). UV-A can inactivate DNA repair
enzymes such as photolyase (Tyrrell et al. 1973) and
glycosylases (Eiberger et al. 2008). However, the main cause
of cell death is DNA molecule alteration.
As observed, there are many forms of UV-induced damage
determining the microbial lethality of UV treatments.
Nevertheless, microbial survivability against UV light is also
dependent on the cells' capacity to repair damage. As there are
many different types of UV-induced DNA damage, microor-
ganisms have developed several pathways for DNA repair.
DNA Repair Mechanisms
DNA repair pathways are classified according to temporal
intervention (prior, during, or after replication) and action
mechanism. Three main pathways are involved in DNA re-
pair: (1) reverse damage repair and (2) excision repair
systems, which act before cell replication occurs, and (3)
tolerating damage pathways, which are activated once repli-
cation has started or immediately afterward. The main DNA
repair pathways are briefly described below and presented in
Fig. 3.
The first group of repair mechanisms restores the DNA
molecule before replication, with remarkable precision and
speed. However, when DNA damage remains unrepaired,
DNA polymerase III (Pol III), the enzyme responsible of
DNA replication, is blocked, and the SOS response to DNA
damage is activated (Bichara et al. 2011). The SOS response is
a global regulatory network governed by the nucleofilament
RecA (comprising RecA proteins and single-stranded DNA),
which stimulates cleavage of the LexA repressor. This induces
the transcription of more than 40 genes involved in cell
division delay, alternative repair mechanisms, and tolerating
lesion pathways, permitting replication (Janion 2008).
Reverse damage mechanisms are carried out by DNA
lyases, which restore the damaged part of the molecule in situ,
without DNA synthesis. In general, two kinds of DNA lyases
can be distinguished in bacteria: CPD lyases (also called
photolyases in the mechanism known as “photorepair”) and
SP lyase. CPD lyases are enzymes responsible for photoreac-
tivation in vegetative bacteria cells, acting specifically against
CPDs using the energy of visible light (350–500 nm). That is,
visible light is necessary for them to act (Sinha and Hader
2002). SP lyase is the main enzyme of SP repair in spores,
acting during spore germination (Setlow 2006). It does not
require visible light. Besides the SP lyase mechanism, SP can
be removed by excision repair or RecA-mediated pathways,
which play minor roles in germinating spore repair (Moeller
et al. 2007).
Excision repair mechanisms replace damaged DNA by
resynthesizing nucleotides. They are considered error-free
mechanisms because excised nucleotides are replaced by
DNA polymerase I (Pol I) using the parental strand as a
template. There are two types of excision repair: base excision
repair (BER), which first removes the damaged base, leaving
an apurinic/apyrimidinic site that is then removed; and nucle-
otide excision repair (NER), which directly removes the nu-
cleotide tracts containing lesions. The key enzymes involved
in BER are DNA glycosylases that recognize specific lesions
in nitrogen bases and excise them. An example of DNA
glycosylase is the endonuclease V or pyrimidine dimer DNA
glycosylase, normally present in UV-resistant microorganisms
such as Micrococcus luteus, Escherichia coli phage T4, and
Saccharomyces cerevisiae (Jacobs and Schaer 2012). NER
can remove a broad spectrum of DNA lesions through multi-
ple cascade reactions carried out primarily by the UvrABC
exinuclease (reviewed in Truglio et al. 2006). NER carried out
by constitutive UvrABC complex is also referred to as “dark
repair” or “liquid holding recovery” (LHR) because UV-
irradiated cells are able to repair their DNA suspended in
Food Bioprocess Technol (2014) 7:1–20 5

Visible light
Reverse damage 350-500 nm
CPD photolyase
Photorepair

DNA glycosylase
AP
lyase

BEFORE REPLICATION
AP site
BER

Excision repair
Pol I
UvrB

UvrA UvrA

UvrB
NER
UvrC

CPD SOS regulon

Pol III
SOS response
LexA
T-T
RNAp

RecA
DURING AND POST REPLICATION

RAMER

Pol III Pol II, Pol IV (non-mutagenicTLS)

TLS Pol III

Pol V (mutagenicTLS)

Homologous recombination

PRR

Fig. 3 DNA repair mechanisms in vegetative cells

minimal medium without the presence of light (Ganesan and TLS occurs during replication and consists of the misin-
Smith 1968). corporation of nucleotides into the synthesized strand opposite
DNA damage tolerance and repair mechanisms induced the lesion by specialized polymerases, giving rise to mutations
after replication activation include RecA-mediated excision (Sinha and Hader 2002). Once the lesion is bypassed, Pol III
repair (RAMER), translesion DNA synthesis (TLS), and post- regains control of the replication. TLS is carried out primarily
replication repair (PRR) (reviewed in Bichara et al. 2011). The by three SOS-inducible DNA polymerases. The first two
activities of all of these mechanisms are regulated thoroughly are Pol II and Pol IV, which are induced at the early stages
in the temporal space by the SOS regulon to safeguard ge- of the SOS response due to their high error-free activity
nome integrity. (nonmutagenic TLS). The third is Pol V (UmuDC complex),
One of the first such mechanisms to be induced is NER which has a high mutagenic activity (mutagenic TLS) and,
mediated by the action of RecA protein (RAMER). When consequently, low error-free activity. Pol V is activated in the
there is extensive damage, the expression of UvrABC latest stages of the SOS response as a last resort to recover cell
exinuclease genes under SOS regulon control (uvrA and viability (Bichara et al. 2011).
uvrB) is reinforced. This provides an effective second oppor- Finally, when a lesion persists, the blockage of Pol III may
tunity for NER to remove lesions, with the help of Rec family lead to the formation of gaps or discontinuities in the daughter
proteins (Courcelle et al. 1999). strand. These gaps are filled after replication by homologous
6 Food Bioprocess Technol (2014) 7:1–20
recombination, a process which is also mainly controlled by
RecA (Sinha and Hader 2002). This mechanism has been
referred to as PRR.
Generally, the action of error-free excision repair pathways
predominates over tolerating mechanisms to avoid their po-
tentially detrimental effects and thereby maintain genetic sta-
bility (Bichara et al. 2011). For instance, Bichara et al. (2007)
reported that when DNA lesions were induced in E. coli by the
chemical carcinogen N-2-acetylaminofluorene, 80 % of the
surviving colonies benefited from RAMER activity. The
remaining colonies (20 %) survived through homologous
recombination mechanisms, predominating over mutagenesis
TLS.
Thus, many mechanisms can act to repair UV-induced
DNA damage. The effects of these mechanisms on microbial
survivability after UV light treatment vary depending on re-
covery conditions (“Recovery Conditions After Processing”
section) and could affect microbial resistance and the kinetics
of inactivation to a great extent. For example, after UV treat-
ment, it has been observed that 99.99 % of the damaged
population of some strains of E. coli can recover in the pres-
ence of visible light (2 mW/cm2 at 360 nm for 3 h) (Kashimada
et al. 1996). Therefore, it is essential to identify the main
parameters affecting UV resistance and how damage and repair
mechanisms may influence microbial resistance to UV light.
Factors Influencing Microbial Resistance to UV Light
Several factors determine microbial inactivation through UV
light. These can be essentially classified as process parame-
ters, microbial characteristics, and product parameters
(Table 1). An adequate knowledge of these factors and their
influence on bacterial death or survivability is necessary to
obtain quality UV inactivation data, as well as to prevent
experimental artifacts and avoid misinterpreting results.
Process Parameters
The main process parameters affecting microbial resistance to
UV light (Table 1) are wavelength emission and UV dose.
Other physical factors could affect microbial resistance, such
as conformation and geometry of the UV equipment, flow
pattern, and optical characteristics of the treatment medium
(López-Malo and Palou 2005). However, these parameters do
not have a direct biological effect on microorganisms, only on
the UV dose received by them. This could result in methodo-
logical artifacts interfering with the correct determination of
microbial inactivation kinetic parameters.
UV effectiveness on microbial inactivation is dependent on
the wavelength emission. Higher lethal efficacy is achieved at
wavelengths closer to DNA's absorption peak. The wavelength
emission depends on the UV lamp used to apply the treatment.
Most conventional UV lamps used for hygienization in the
food and water industries are low-pressure (LP) and medium-
pressure (MP) mercury vapor lamps and pulsed xenon (PX)
lamps, technology known as pulsed UV light (PUV)
(Kowalski 2009).
LP lamps emit quasi-monochromatic light at a wavelength
of 253.7 nm (85 % of total lamp emission), close to maximum
DNA absorbance. MP lamps emit a polychromatic spectrum
covering wavelengths from around 200 to 600 nm, with only
15–23 % of emissions at 253.7 nm (Fig. 1) (Kowalski 2009).
MP lamps show the same microbial survival rate as LP lamps
at the same dose, despite the expected damage to other cellular
components because of their polychromatic nature (Oguma
et al. 2004; Eischeid and Linden 2007). For instance, Oguma
et al. (2004) reported that the UV doses required to inactivate
90 % of the initial population of E. coli and Legionella
pneumophila suspended in a phosphate buffer (pH 7.2) using
two LP lamps (20 W) and a MP lamp (330 W) were not
significantly different.
PUV technology has been considered a more rapid and
effective method of microbial inactivation than continuous
UV irradiation due to the use of intense, short duration
pulses across a broad spectrum (100–1,100 nm) (Fig. 1).
The main cause of PUV inactivation is also believed to be
DNA damage caused by UV wavelengths (approximately
54 % of emitted energy), although concomitant mechanisms
may contribute to improving its effectiveness (Demirci and
Krishnamurthy 2011). In addition to photochemical DNA
damage, photothermal effects and photophysical effects have
been also described. Photothermal effects are attributed to the
temporary intracellular overheating caused by the absorption
of photons, especially from UV-A and UV-B, when high
fluence is applied (Wekhof et al. 2001). Wekhof (2000) mea-
sured the temperature of E. coli cells treated by different PUV
treatments. Applying a fluence of 0.5 J/cm2, cell temperature
momentarily rose, reaching values higher than 120 °C.
Photophysical effects refer to the disruption of cell membranes
and other cell components. The origin of these alterations is
not clear, but some authors have suggested that they are
consequences of temperature increases in bacteria and sur-
rounding media (Wekhof et al. 2001; Takeshita et al. 2003).
More investigation is needed to elucidate PUV technology's
actual mechanism of microbial inactivation.
The colony-forming viability of bacteria, as well as the
total DNA damage, is highly correlated with the applied UV
dose (Oguma et al. 2004; Eischeid and Linden 2007).
However, the inactivation kinetics described in the literature
do not always follow the same pattern when the microbial
inactivation, expressed in logarithmic units, is represented
against the UV dose (survival curve). Some authors (Oteiza
et al. 2010) have described the UV survival curves using first-
order kinetics, where the number of viable cells decreases
exponentially when a constant dose is applied:
Food Bioprocess Technol (2014) 7:1–20 7

Table 1 Classification of
influencing factors on microbial Process Microbial characteristics Product parameters
resistance to UV light. Small let- parameters
ters (from a to c) indicate the rel-
ative relevance of each factor Dose (c) Intrinsic factors pH
(a—none, non-influence; Wavelength (c) Type (c) Cell wall thickness aw
b—relevant; c—very relevant) Specie (b) Cell size Absorption
coefficient (c)
Strain (c) Pigmentation Turbidity (b)
DNA molecule
(size, composition,
compaction)
Efficiency of repair
mechanisms
Membrane fluidity
Extrinsic factors
Growth phase (b)
Growing conditions
Medium composition (a)
Temperature
Stresses
Oxidative shock (a)
Acid shock (b)
Basic shock (a)
Osmotic shock
Heat/IR shock (c)
Starvation stress (b)
Visible light (b)
UV (homologous protection)
Recovery conditions
Medium composition (a)
LHR (a)
Photoreactivation (c)

LnðN =N 0 Þ ¼ e−kd
where N and N0 are the number of microorganisms for any
treatment dose (d) and at the beginning, respectively, and k is
the inactivation rate constant. Considering conventional heat
treatments, a decimal reduction dose (DUV) can also be defined
as the dose necessary to reduce 90 % of the initial population,
and this is equal to 2.303/k. DUV values are commonly used to
characterize the UV sensitivity of microorganisms.
First-order kinetics is characterized as a one-hit process,
assuming that the death of microorganisms is due to a single
event (the reaction of one UV photon) involving a vital target
(DNA molecule) and that all cells have an identical probability
of death (Quintero-Ramos et al. 2004). However, in UV
survival curves, the results often deviate from linearity, show-
ing shoulders, tails, or both (Sastry 2000). According to the
multi-hit single target theory, the shoulder phase is related to
damage and DNA repair phenomena: Various photon events
have to affect the bacterial chromosome until the number of
lesions exceeds the capability of DNA repair mechanisms
(Quintero-Ramos et al. 2004; López-Malo and Palou 2005).
Once these repair mechanisms are overcome, minimal addi-
tional UV exposure would be lethal for microorganisms, and
the number of survivors would rapidly decline. This is
evidenced by DNA repair-deficient strains, for which survival
curves show a great reduction in the shoulder phase, accom-
panied by an increased slope within the log-linear region
(Ganesan and Smith 1968). On the other hand, the upward
concavity means that the process is becoming progressively
less efficient with the applied dose. The tailing phase can be
explained by the existence of subpopulations with different
UV resistance and cell aggregates, as well as associations with
particles in the liquid medium (Mamane-Gravetz and Linden
2005; Velez-Colmenares et al. 2011).
These biological causes should be distinguished from those
produced by the lack of homogeneous dose distribution in the
reactor, which is related to the high absorbance or presence of
8 Food Bioprocess Technol (2014) 7:1–20

Table 2 UV doses required for 90 % reduction of the initial population The type of UV system (bench scale or continuous flow system) and UV
(DUV values) of different types of microorganisms, species, and strains source (number of lamps, type of lamps, and the total input power) used
reported in water and laboratory media. DUV values were expressed in to obtain data are included
fluence unit (millijoules per square centimeter), except where indicated.

Microorganism Treatment medium UV system UV source DUV (mJ/cm2) Reference

Candida albicans ATCC 10231 Buffer Bench scale LP (17 W) 44.7 Abshire and Dunton (1981)
Micrococcus radiodurans ATCC 13939 198.6
Enterococcus faecalis ATCC 10541 12.0
Staphylococcus aureus ATCC 6538 5.6
Escherichia coli ATCC 8739 8.1
Pseudomonas cepacia ATCC 25416 5.2
Pseudomonas diminuta ATCC 11568 11.9
Pseudomonas diminuta ATCC 19146 7.4
Pseudomonas aeruginosa WB-1 5.8
Pseudomonas aeruginosa G-2 3.0
Pseudomonas aeruginosa ATCC 10145 4.6
Acanthamoeba castellanii ATCC 30234 Wastewater NA NA 60 Chang et al. (1985)a
Rotavirus SA-11 7.1
Bacillus subtilis ATCC 6633—spores 36
Enterococcus faecalis ATCC 29212 6.6
Staphylococcus aureus ATCC 25923 3.9
Escherichia coli ATCC 11229 3.0
Salmonella typhi ATCC 6539 2.7
Bacillus subtilis DE69 PBS Sunlight MP 3.2 Wassmann et al. (2011)
Vegetative cells
Spores Simulator SOL 2 14.2
Escherichia coli O157:H7 CCUG 29193 Buffer Bench scale 10× LP (36 W) 3.5 Sommer et al. (2000)a
Escherichia coli O157:H7 CCUG 29199 0.4
Escherichia coli O25:K98:NM 5
Escherichia coli ATCC 11229 3.5
Cryptosporidium parvum Water and wastewater MP 4.4 Hijnen et al. (2006)b
Girdia muris MP 8.2
Acanthamoeba spp. MP 47.6
Bacillus subtilis—spores MP 16.9
Clostridium perfringens—spores LP 16.7
Estreptococcus faecalis MP 3.2
Legionella pneumophila MP 2.5
Escherichia coli MP 1.8
Salmonella typhi MP 1.9
Campylobacter jejuni MP 1.1
Yersinia enterocolitica MP 1.1
Vibrio cholerae MP 0.7
Enterococcus faecium NUIG J952 TSYEA Bench scale PX 4.2c Farrell et al. (2010)
Enterococcus faecalis NUIG D46209 3.4c
Enterobacter sakazakii NCTC 8155 2.1c
Staphylococus aureus NUIG 5624 2.0c
Listeria monocytogenes NUIG 11994 2.6c
Escherichia coli DIT 02B1173 2.0c
Klebsiella pneumoniae DIT 04B4415 1.9c
Pseudomonas aeruginosa NUIG 2605 2.7c
Pseudomonas aeruginosa NUIG R5137 1.5c
Pseudomonas aeruginosa NUIG 2633 2.4c
Food Bioprocess Technol (2014) 7:1–20
Table 2 (continued)
Microorganism Treatment medium
Pseudomonas aeruginosa DIT 02B710
NA data not available, LP low-pressure mercury vapor lamp, MP medium-pressure mercury vapor lamp, PX pulsed xenon lamp
a
Data estimated by Cairns (2006)
b
Values were estimated from different inactivation data from literature obtained using bench scale or continuous flow systems with one or more LP or
MP lamps
c
DUV values are expressed in number of light pulses (energy discharge 7.2 J)
suspended solids in liquid foods, high microbial concentra-
tion, and the shading effect from surface irregularities in a
solid matrix (Koutchma 2009). For example, in some studies
applying UV light to surfaces, survival curves with tails have
been observed (Schenk et al. 2008). It is important to distin-
guish tailing phenomena from artifacts resulting from errors in
the methods used for enumerating survivors.
One of the consequences of the absence of linearity in the
survival curves is the difficulty of obtaining a parameter to
describe inactivation kinetics and compare results. To solve this
problem, authors have described survival curves with different
mathematic nonlinear equations, such as the Weibull, Gompertz,
Geeraerd, and log-logistic models (Quintero-Ramos et al. 2004;
Unluturk et al. 2010; Gayán et al. 2011). However, there is no
agreement about the most adequate model to fit these deviations,
and this consensus is necessary to compare results and accurate-
ly calculate processing parameters for effective hygienization.
Microbial Characteristics
Microbial resistance to UV light has been found to depend on
both intrinsic and extrinsic factors (Table 1).
Intrinsic Factors
UV resistance varies widely by the type of microorganism,
species, and strain. Tables 2 and 3 show some UV resistance
data from the literature based on laboratory media, water, and
liquid food to illustrate this variability. Frequently, comparing
data obtained by different authors is risky because of the
different conformations and geometry of UV light equipment,
flow or stir patterns, and the optical properties of the liquid
media used, as well as discrepancies in the expression and
calculation of the applied doses. For this reason, methodolog-
ical elements used to obtain the resistance data were included
in the tables.
According to Table 2, vegetative bacteria are the most
sensitive, followed by yeast, bacterial spores, viruses, and
protozoa. Inside the bacterial group, Gram-positive bacteria
generally show more UV resistance than Gram-negatives, but
this is not a general rule. Enterococcus spp. are considered one
9
UV system UV source DUV (mJ/cm2) Reference
2.6c
of the most tolerant water-related pathogens to UV-C and PUV
(Abshire and Dunton 1981; Chang et al. 1985; Hijnen et al.
2006; Farrell et al. 2010). On the contrary, Staphylococcus spp.
have often shown similar or greater sensitivity to UV technol-
ogy than coliforms (Abshire and Dunton 1981; Chang et al.
1985; Hijnen et al. 2006). However, the variability in UV
resistance among species and strains is larger than the diver-
gences among genera, which avoid general conclusions
(Table 2). For instance, Abshire and Dunton (1981) reported
that the resistance to UV-C of Enterococcus faecalis (ATCC
10541) was 2.1 times higher than that of Staphylococcus au-
reus (ATCC 6538). However, the DUV values of Pseudomonas
spp. strains varied up to 4.0 times. Similarly, Farrell et al.
(2010) observed that the difference in resistance to PUV be-
tween E. faecium (NUIG J952) and S. aureus (NUIG 5624)
was 2.0 times, whereas variations observed among P.
aeruginosa strains were of the same order of magnitude.
Higher divergences in UV-C resistance have been observed
among enteropathogenic E. coli strains, with varying DUV
values almost 13 times (Sommer et al. 2000). Due to the great
variability in UV resistance among strains, the Environmental
Protection Agency's Scientific Advisory Panel has recom-
mended establishing UV-C irradiation process criteria for water
disinfection by testing five outbreak-related strains in a cocktail
for each pathogen (Oteiza et al. 2010).
Data on UV effectiveness against most significant food-
borne pathogenic and spoilage bacteria are still limited.
Listeria monocytogenes is considered one of the most UV-
resistant foodborne pathogens in milk (Lu et al. 2011) and
fruit juices (Guerrero-Beltrán and Barbosa-Cánovas 2006;
Gabriel and Nakano 2009). On the other hand, Salmonella
spp. are one of the most sensitive genera (Gabriel and Nakano
2009; Lu et al. 2011). For instance, Gabriel and Nakano
(2009) reported a DUV value for L. monocytogenes (HCIPH
AS-1) 2.1 times higher than for Salmonella typhimurium
(ATCC 12529) in apple juice (Table 3). Nevertheless, a wider
variability in UV resistance among strains of pathogenic bac-
teria has been detected (Table 3), which may explain some
discrepancies in the literature when comparing the relative
resistance of species. A variation in DUV values of up to 5.5
times among E. coli O157:H7 strains have been observed
10 Food Bioprocess Technol (2014) 7:1–20

Table 3 UV doses required for 90 % reduction of the initial population UV system (bench scale or continuous flow system) and UV source
(DUV values) of different types of microorganisms, species, and strains (number of lamps, type of lamps, and the total input power) used to
reported in liquid foods. DUV values were expressed in fluence unit obtain data are included
(millijoules per square centimeter), except where indicated. The type of

Microorganism Treatment medium UV system UV source DUV (mJ/cm2) Reference

Saccharomyces cerevisiae BFE-39 Apple juice Bench scale 2× LP (15 W) 6.4a Gabriel (2012)
Debaryomyces hansenii BFE-34 8.3a
Clavispora lusitaniae BFE-36 9.8a
Torulaspora delbrueckii BFE-37 9.4a
Pichia fermentans BFE-38 11.4a
Escherichia coli O157:H7 CR-3 2.8a
Escherichia coli O157:H7 HCPIH-96055 0.5a
Listeria monocytogenes HCIPH AS-1 Apple juice Bench scale 2× LP (15 W) 1.26a Gabriel and Nakano (2009)
Listeria monocytogenes HCIPH M24-1 0.44a
Escherichia coli O157:H7 0.5a
Escherichia coli K12 0.6a
Salmonella typhimurium ATCC 12529 0.61a
Salmonella enteritidis HCIPH B11 0.27a
Saccharomyces cerevisiae Apple juice Thin film flow reactor 2× LP (25 W) 12.2 Guerrero-Beltrán and
Listeria innocua 4.9 Barbosa-Cánovas (2006)
Escherichia coli 2.9
Escherichia coli O157:H7 (303/00) Orange juice Bench scale 4× LP (30 W) 296 Oteiza et al. (2010)
Escherichia coli O157:H7 (749/03) 169
Escherichia coli O157:H7 (547/03) 210
Escherichia coli O157:H7 (33/98) 168
Escherichia coli O157:H7 (EDL 933) 212
Saccharomyces cerevisiae DSM 70478 Apple juice Coiled tube (Vivatec) LP (8 W) 2.6b Müller et al. (2011)
Alyciclobacillus acidoterrestris DSM 1.3b
2498—vegetative cells
Escherichia coli DH5α 0.5b
Lactobacilllus plantarum BFG 5092 0.3b
Lactococcus lactis (cocktail) Whole milk Coiled tube LP (80 W) 5.1 Lu et al. (2011)
Listeria monocytogenes (cocktail) 3.5
Escherichia coli (cocktail) 3.5
Salmonella typhimurium (cocktail) 3.4
Staphylococcus aureus (cocktail) 3.2
Pseudomonas aeruginosa (cocktail) 3.3

LP low-pressure mercury vapor lamp, MP medium-pressure mercury vapor lamp, PX pulsed xenon lamp
NA data not available, LP low-pressure mercury vapor lamp, MP medium-pressure mercury vapor lamp, PX pulsed xenon lamp
a
Data estimated by Cairns (2006)
b
Values were estimated from different inactivation data from literature obtained using bench scale or continuous flow systems with one or more LP or
MP lamps
c
DUV values are expressed in number of light pulses (energy discharge 7.2 J)

(Gabriel 2012). More examples of UV resistance data for
bacteria in liquid foods are provided in Table 3. Overall, more
investigation into UV resistance in different strains of relevant
pathogens is needed in order to identify the most resistant
microorganisms of public health significance.
Variations observed among microorganisms, species, and
strains have been attributed to different factors, including cell
wall thickness; cell size; pigmentation; composition, size, and
conformation of the genetic material; and DNA repair efficien-
cy. For example, the higher UV resistance of Gram-positive
versus Gram-negative bacteria has been related to the thicker
peptidoglycan cell wall of the former, which may hinder the
penetration of UV light photons within cells (Beauchamp and
Lacroix 2012).
Comparing the same genetic material content, larger sized
cells are more resistant to UV light because there is a higher
Food Bioprocess Technol (2014) 7:1–20
probability of photons being absorbed by other compounds
before affecting DNA (Oteiza et al. 2010; Gabriel 2012). This
is one of the reasons molds and yeasts are more resistant than
bacteria (Tables 2 and 3). In addition, the lower pyrimidine
content in the DNA composition of yeast may also contribute
to its higher UV resistance (Fredericks et al. 2011).
Apart from DNA composition, the extent of UV damage
has been also correlated with genome size. Müller et al. (2011)
attributed the larger UV-C resistance of S. cerevisiae compared
to Lactobacillus plantarum to higher cellular DNA content
(Table 3). However, haploid yeasts appear to be more sensitive
to UV-C radiation than their diploid form (Rodrigues et al.
2003), probably because target genes are present in several
copies, decreasing the probability of all copies being hit.
DNA condensation also protects against UV damage.
Deinococcus and Rubrobacter genera have strong UV resis-
tance, which is partly attributable to their stronger genome
condensation compared with the uniform E. coli nucleoid
(Blasius et al. 2008).
Differences in intrinsic repair efficiency may also contribute
to the variations in UV survival among microorganisms. Cheig
et al. (2012) attributed the greater UV-C and PUV sensitivity of
E. coli O157:H7 compared to L. monocytogenes to its smaller
DNA repair activity, since their quantitative analysis of DNA
damage showed that the CPD formation in E. coli O157:H7 was
slightly greater than in L. monocytogenes. Similarly, Suss et al.
(2009) observed that the higher UV-C recovery of P. aeruginosa
in comparison to a UV-sensitive strain of Enterococcus faecium
was correlated with intensive repair in the former, whereas no
DNA repair was detected in E. faecium.
The physical state (fluidity) of the cell membrane also can
play an important role in UV resistance because bacterial
chromosomes interact with the cytoplasmic membrane. Some
agents involved in DNA repair mechanisms (RecA and Uvr
proteins) are attached to the membrane to perform their func-
tions (Lin et al. 1997). It has been reported that excision repair
is modulated by the fluidity of the cell membrane in UV-C-
irradiated E. coli cells (Todo et al. 1983).
Finally, pigmentation is believed to protect cells by absorb-
ing light at UV wavelengths and scavenging free radicals
generated by UV-A (Moeller et al. 2005). Thus, pyocyanin
and pyoverdine pigments protect P. aeruginosa against UV
light (Burke et al. 1990; Farrell et al. 2010). However, this
point should still be addressed because contradictory results
have been found concerning the UV-protective role of pigmen-
tation (Turtoi and Nicolau 2007; Khaneja et al. 2010).
Bacterial spores are well known for their great UV resis-
tance properties. For example, spores of various Bacillus spe-
cies are five to 50 times more resistant to UV radiation than
vegetative cells (Setlow 2001). This high resistance has been
ascribed to several mechanisms: the relatively dehydrated state
of the spore core reducing the probability of pyrimidine dimer-
ization, the effective action of SP lyase during germination, the
11
accumulation of a high percentage of dipicolinic acid in the
dormant spore core (Slieman and Nicholson 2001), and the
presence of a thick spore protein coating (Riesenman and
Nicholson 2000). Finally, spores like Bacillus spp. are able to
produce a broad spectrum of pigments, especially carotenoids,
during germination, which could provide some UV-A protec-
tion (Moeller et al. 2005; Khaneja et al. 2010).
Extrinsic Factors
Among extrinsic factors influencing UV microbial resistance,
the main ones are the growth phase, growing conditions,
stressors prior to UV treatment, and recovery conditions after
processing.
Growth Phase The life cycle of bacteria includes periods of
growth at various rates interspersed with periods of nongrowth,
depending on the availability of nutrients. UV resistance may
vary during these times. Several authors have reported that
stationary-grown cells in various bacterial species show en-
hanced UV resistance compared to actively growing cells.
For instance, Child et al. (2002) reported that the resistance of
mid-exponential phase cells of S. typhimurium grown in a
complete rich medium under UV-C (70 J/m2, UV Stratolinker
apparatus) in a buffer (pH 7) increased by more than 1.3 Log10
cycles at the start of the stationary phase of growth. Most of
these studies were performed in batch cultures where changes
in other factors such as medium composition might have
hidden the effect of the growth phase on UV sensitivity
(Berney et al. 2006). Systematic studies of the effect of specific
growth rate on E. coli's UV resistance have been conducted
using continuous cultures and show that the specific growth
rate is strongly correlated with UV resistance (Berney et al.
2006; Bucheli-Witschel et al. 2010). Bucheli-Witschel et al.
(2010) reported that bacteria cultivated in glucose-MM at
intermediate specific growth rates between 0.2 and 0.4 h−1
exhibited the lowest UV-C resistance and that it increased
above and below these values. The difference in inactivation
levels between stationary growth cells of E. coli and cells
grown in the chemostat culture at dilution rates of 0.02, 0.22,
and 0.58 h−1 treated by UV-C (50 J/m2, bench scale device, 4×
LP lamps—16 W) in the same growth medium were 0.5, 2.4,
and 0.9 Log10 cycles, respectively. Considering that in batch
cultures, the specific growth rate decreases constantly until the
stationary growth phase is reached, UV-C resistance decreased
during the mid-exponential phase and reached maximum resis-
tance just before cells entered the stationary phase.
In Gram-negative bacteria, the increase in UV resistance
along with the progressive growth rate decrement has been
related to the induction of the general stress response sigma
factor RpoS (σ38) (Child et al. 2002; Berney et al. 2006;
Bucheli-Witschel et al. 2010). Bucheli-Witschel et al. (2010)
reported that RpoS is involved in the UV-C resistance of
12
growing E. coli cells at low rates (0.2–0.3 h−1) but not at
medium or high rates. This corresponds with the increase in
RpoS expression when the growth rate decreases (Ihssen and
Egli 2004). However, the sensibility of exponential phase cells
cannot be explained simply by the low expression of RpoS
factor (Child et al. 2002; Bucheli-Witschel et al. 2010).
Although there are some indications that relate the RpoS
factor to the action of the nucleotide excision repair system
(Tyrrell et al. 1972), a direct relationship has not yet been
found yet. A possible link between the RpoS factor and UV-C
resistance might be the induction of the expression of DNA-
binding proteins (Dps). Dps bind to the chromosome, forming
a stable nucleoprotein complex which may change DNA
reactivity toward UV-C irradiation and increase the efficiency
and accuracy of repair mechanisms (Nair and Finkel 2004).
For high specific growth rates (>0.4 h−1), the decrease of
UV-C sensitivity in E. coli as the growth rate increases has
been related to expanding genome content. Bronk and
Walbridge (1980) reported that the increase of UV-C resis-
tance in exponential phase cells was due to the lengthening of
the shoulder phase of survival curves when DNA content was
augmented. According to the multiple target theory, this can
be attributed to the enhancement of a number of target mole-
cules (Bronk and Walbridge 1980). In other words, the incre-
ment of DNA content per cell may imply that a target gene is
present in several copies, and therefore, it is less likely that all
copies will be hit and damaged (Bucheli-Witschel et al. 2010).
Also, high activation of repair systems mediated by RecA due
to an increase in the number of replication forks could be
involved (Dri and Moreau 1993).
In Gram-positive bacteria, the effect of the growth phase has
not been studied, with the exception of B. subtilis (Wassmann
et al. 2011). The obtained results were the opposite of the
general assumption that exponentially growing cells are more
sensitive to UV light than stationary-grown cells. The DUV
value of exponential phase cells of B. subtilis DE69 (2.4 h of
growth in nutrient broth) treated under a UV polychromatic
lamp (200–400 nm, Sunlight Simulator SOL 2) in a buffer (pH
7) was almost two times higher than that of stationary phase
cells. This suggests that the expression of the stress sigma
factor B (SigB/σB) at the start of the stationary growth phase
is not involved in UV resistance. In fact, preliminary studies
from the same authors showed that the UV resistance of
stationary phase cells of a B. subtilis wild-type strain was
almost identical to that of an isogenic σB mutant.
It is well known that during the stationary phase of bacterial
growth, new genotypes appear through random spontaneous
mutation (Dykhuizen 1999; Vulic and Kolter 2001). Genotypes
that can confer a competitive advantage in nutrient-poor con-
ditions are selected, encouraging subpopulations of different
phenotypes (Vulic and Kolter 2001), which may have UV
sensitivity that differs from the initial population. Child et al.
(2002) observed that the inactivation of stationary-grown cells
Food Bioprocess Technol (2014) 7:1–20
of S. typhimurium subjected to prolonged incubation in batch
cultures for 2 months showed a regular cycling of UV-C
resistance fluctuations, varying nearly 3 three Log10 cycles at
a UV-C dose of 100 J/m2. Although RpoS is not involved in
UV survivability at the late stationary growth phase (Child et al.
2002; Bucheli-Witschel et al. 2010), it is indirectly related
because it increases the mutation rate. RpoS stabilizes Pol IV
in the stationary growth phase and also downregulates enzymes
responsible for mismatch repair (Foster 2007). Mutations may
result in the appearance of UV-tolerant subpopulations that do
not remain stable during prolonged incubation.
In summary, to draw concise conclusions when comparing
the UV resistance of different microorganisms or the influence
of related factors, it is necessary to specify the age of bacterial
cultures. From a microbiological point of view, it would be
very interesting to thoroughly study the effects of growth
phases on the UV resistance of different microbial groups
and to determine the intrinsic factors that could affect it.
Growing Conditions There is little data related to the growth
factors influencing microbial UV resistance; growing medium
composition and growth temperature are the primarily studied
parameters. Some authors have reported that cells grown in
media with simple molecules arabinose or glycerol as carbon
sources were more UV-C sensitive than those grown in glu-
cose media (Rude and Alper 1972; Schenley et al. 1976).
Schenley et al. (1976) demonstrated that the UV survivability
of glucose-grown cells was higher than those grown in glyc-
erol due to higher excision repair activity. These data suggest
that the metabolic activity of growth prior to UV irradiation
determines the efficiency of DNA repair and thus UV resis-
tance. However, the medium composition only varied the UV-
C sensitivity of E. coli by 25 % (Schenley et al. 1976).
Regarding bacterial spores, it has been reported that spor-
ulation conditions influence UV resistance. Bacillus spp.
spores purified from soil exhibited two to three times higher
resistance than B. subtilis spores grown in laboratory media
(Nicholson and Law 1999). Therefore, giving precise indica-
tions regarding the composition of growth and sporulation
media is strongly recommended.
On the other hand, several have reported that indigenous
food microorganisms are more resistant to UV technology than
are pure cultures (Franz et al. 2009; Lu et al. 2011). For
instance, UV-C treatment of raw milk at 10.7 mJ/cm2 applied
by a coiled tube reactor only reduced 2 Log10 cycles of the
native microorganisms, including Staphylococcus spp., Listeria
spp., Salmonella spp., and Pseudomonas spp. Meanwhile, the
same dose was able to inactivate more than 3 Log10 cycles of
each pure culture inoculated in milk. To explain these differ-
ences, the existence of subpopulations of native microorgan-
isms with UV resistance genes turned on was proposed.
Variations in growth temperature induce changes in the
membrane fatty acid composition of microorganisms to
Food Bioprocess Technol (2014) 7:1–20
maintain a degree of fluidity compatible with life (Casadei
et al. 2002). Therefore, since cytoplasmic membrane fluidity
has an essential role in DNA repair (Todo et al. 1983; Lin et al.
1997), growth temperature could be a crucial factor in UV
resistance. However, the available data indicate that stationary
phase cells of Cronobacter sakazakii (Arroyo et al. 2012b)
and E. coli K12 (unpublished data) grown at 10 and 37 °C
showed the same degree of UV-C resistance.
Stresses Prior to UV Treatments During food processing,
bacteria may be exposed to stress conditions which can pro-
duce DNA damage or interfere with replication, activating the
SOS response (van der Veen and Abee 2011). As a conse-
quence, cross-protection against subsequent UV treatments
could occur. A great number of stressors encountered in some
food processing steps such as heat, acid, alkali, oxidative,
osmotic, starvation, and ethanol have been shown to increase
UV resistance. In some cases, their effect is noticeable, increas-
ing UV resistance up to 3.5 times after heat shocks (Pardasani
and Fitt 1989). This cross-protection is controlled by regulators
that induce the expression of multiple genes which aid micro-
bial adaptation: alternative sigma factors (RpoS and RpoH in
Gram-negative bacteria and sigB in Gram-positive ones), small
molecule effectors such as guanosine 5′-diphosphate 3′-di-
phosphate (ppGpp), gene repressors such as LexA, and inor-
ganic molecules such as polyphosphates (Foster 2007).
Although the biology of stress responses in traditional food
hurdles has been widely studied, with regard to UV processing,
there is little and contradictory information.
Exposure to oxidative agents such as hydrogen peroxide
and sodium hypochlorite induces the intracellular formation
of ROS, causing DNA damage and activating the SOS re-
sponse (van der Veen and Abee 2011). For instance, previous
exposure to oxidative stresses (2.5 mM H2O2 for 20 min)
increased the UV-C survivability of E. coli cells treated at 12
mJ/cm2 by around 0.5 Log10 cycles (Asad et al. 1994). This
protection involves the induction of some DNA repair mech-
anisms dependent on RecA and UvrA proteins (Asad et al.
1994). On the contrary, oxidative shock (H2O2 0.5 mM for 1
h) sensitized C. sakazakii to UV-C (Arroyo et al. 2012a).
Exposure to mildly acidic conditions (pH 5 for 3 h) provided
cross-protection to L. monocytogenes against UV-C light,
increasing survivability by 2.2 Log10 cycles in distilled
water after 20 min of irradiation (12.8–33.2 mJ/cm 2 )
(McKinney et al. 2009). Similarly, the inactivation rate of L.
monocytogenes to PUV light (7.2 μJ/cm2) decreased 25 %
after an acid shock of pH 5.5 for 5 h (Bradley et al. 2012).
However, no changes in the UV-C resistance of acid-stressed
C. sakazakii (Arroyo et al. 2012a) or Lactococcus lactis
(Hartke et al. 1995) cells were observed. Acid exposure results
in DNA strand breaks, and the acid sensitivity increases in
RecA-deficient strains, highlighting the role of the SOS sys-
tem in acid resistance (van der Veen and Abee 2011).
13
Little information exists concerning the alkaline stress effect
on UV sensitivity. Goodson and Rowbury (1990) observed
that the inactivation of E. coli and its RecA-deficient derivative
grown in nutrient broth of pH 9.0 was 53 % lower after 60 s of
UV-C irradiation than in those microorganisms grown at neu-
tral pH. This could be explained by the inactivation of LexA
repressor under alkaline conditions (Little 1991). In contrast,
UV-C resistance of C. sakazakii was significantly reduced (20
%) after an alkaline shock at pH 9 for 1 h (Arroyo et al. 2012a).
Exposure to high salt concentrations results in the modulation
of the structural conformation of RecA to an activated state
(Dicapua et al. 1990), which could turn on the SOS response
and boost microbial UV resistance. However, osmotic shocks
did not change the sensitivity of L. monocytogenes to PUV (7.5
% NaCl for 1 h) (Bradley et al. 2012) or of C. sakazakii to UV-
C (5 % NaCl for 1 h) (Arroyo et al. 2012a). Alternatively, pre-
irradiation of E. coli cells with monochromatic visible light at
wavelengths of 446, 466, 495, and 685 nm for 30 min in-
creased UV-C cell survivability (12 mJ/cm2) by almost 1 Log10
cycle (Lage et al. 2000).
Heat shock (HS) is one of the most studied stressors that
could affect microbial survivability to UV light. For instance,
HS at 42 °C for 45 min increased the UV-C survivability (35–
60 J/m2) of E. coli up to 3.5 times (Pardasani and Fitt 1989).
Similarly, Lage et al. (2000) observed a decrease of 1.9 Log10
cycles in the UV-C inactivation (120 J/m2) of E. coli when cells
were pre-irradiated with polychromatic infrared radiation (60
min). This was attributed to the localized temperature increases
within the cellular environment. The UV resistance increments
after HS are related to the stimulation of excision repair via the
SOS response (Pardasani and Fitt 1989). However, other au-
thors noticed no PUV or UV-C survival improvement (Arroyo
et al. 2012a; Bradley et al. 2012). Moreover, L. monocytogenes
(McKinney et al. 2009) and Vibrio cholerae (Jeevan and
Ghosh 1995) became more vulnerable. When bacteria are
subjected to a rapid increase in external temperature, they
respond by expressing heat shock proteins (HSPs) under the
transcriptional control of the alternative sigma factor RpoH
(σ32), increasing their subsequent thermotolerance. HSP re-
sponse overlaps with SOS response by protecting heat-labile
proteins important for DNA repair from degradation (Zou et al.
1998; Layton and Foster 2005).
UV survival improvement after starvation stresses has also
been widely reported. For instance, the UV-C resistance (18
mJ/cm2) of E. coli after 24 h of deprivation of amino acids or
thiamine and glucose increased by about 0.75 and 1.75 Log10
cycles, respectively, in comparison with cells grown in a
complete medium (Fitt and Sharma 1991). In this case, con-
trary to what was expected, the RpoS response under nutrient
limitation conditions hardly contributed to this phenomenon.
The implications of the RpoH response and ppGpp in tempo-
rarily halting DNA replication have been suggested (Sedliakova
1998; Foster 2007).
14
Finally, homologous protection after the application of
low UV doses has been observed, a phenomenon called
photoprotection. Pre-exposure to a near-UV lamp (300–400
nm, 8×104 J/m2) causes DNA lesions that trigger the SOS
response and growth delay as part of the SOS function
(Bhatnagar 1992). On the other hand, low UV doses (50–100
J/m2) induce HSP synthesis (DnaK and GroEL proteins) in E.
coli, contributing to UV resistance improvement (Krueger and
Walker 1984). Similarly, pretreating P. aeruginosa with low-
energy doses of PUV (0.2 J/m2) increased the survivability of
further high intensity PUV treatments (1 J/cm2) by 3 Log10
cycles (Massier et al. 2012). Overall, as the development of
cross-protection against UV light during food processing could
have important consequences in terms of food safety, it is
necessary to obtain deeper knowledge concerning the stressful
conditions that improve microbial UV resistance and under-
stand the causes of existing discrepancies.
Recovery Conditions After Processing Environmental condi-
tions after UV treatment can determine microbial resistance to
a great extent. Bacteria survivability after UV irradiation is
higher when cells are plated on minimal growth medium rather
than on rich growth medium (Ganesan and Smith 1968).
Similarly, cell recovery in a minimal liquid medium in the
dark, that is, so-called liquid holding recovery (LHR), is better
than when the cells are directly plated in complete agar. This
phenomenon has been attributed to NER action before plating
(Ganesan and Smith 1968).
Based on Ganesan and Smith's first hypothesis (1968), the
number of dimers that can be removed by NER depends on
the number of enzymes present in the irradiated cells and the
time available for NER before replication ensues. In complete
growth media, the maximum amount of time available for
NER would be one generation time. If a cell is not able to
remove all dimers, then replicational repair pathways will then
be activated, including error-prone mechanisms. Thus, cells
will have more probability of DNA repair failure, resulting in
nonviable cells. This conjecture was set aside when molecular
techniques appeared, allowing researchers to thoroughly study
the DNA repair pathways. However, from a practical point of
view, it is critical to know which repair mechanisms can occur
in different recovery media, such as food matrices, and espe-
cially to understand their impact on bacteria survivability.
Therefore, these investigations should be reconsidered.
Currently, LHR is important due to the increase in the
number of UV treatment facilities for drinking water and
wastewater treatment throughout the world. Thus, the recov-
ery of pathogens in dark conditions after applying UV doses
now considered safe might make treatment ineffective. The
extension of LHR depends on the intrinsic abilities of each
microorganism, which vary among species and even strains.
For instance, LHR plays no role or a minimal one in E. coli
Food Bioprocess Technol (2014) 7:1–20
recovery (Sommer et al. 2000), with the exception of strain
O50:H7. The UV-C dose required to achieve 6 Log10 reduc-
tions of E. coli O50:H7 in clear buffer increased 1.7-fold
considering LHR (48 h at 22 °C). Pathogenic species in fish
such as Aeromonas spp. and Vibrio spp. are able to carry out
extensive LHR. Aeromonas salmonicida subsp. salmonicida
showed a dark recovery (48 h at 22 °C) of almost 2 Log10
cycles after applying a UV-C dose of 6 mJ/cm2 (3 Log10
cycles of inactivation) (Liltved and Landfald 1996). LHR is
temperature dependent, occurring to a greater extent at 37 °C
than at lower temperatures (4 °C) (Liltved and Landfald
1996). LHR has been well described when microorganisms
are treated in water. However, it has hardly been investigated
in treated foods, which is an essential point in applying UV
technology to food hygienization.
In addition to dark repair, photoreactivation can be an
efficient DNA repair mechanism and much more important
than dark repair (Liltved and Landfald 1996; Sommer et al.
2000). Photoreactivation is crucial for water disinfection when
water is exposed to visible light after UV treatment. However,
it has been poorly considered when microorganisms are treated
in food.
The photorepair capability of microorganisms differs greatly
for different species and strains (Tosa and Hirata 1999; Hassen
et al. 2000; Sommer et al. 2000). This ability depends on
whether the enzyme photolyase gene is present, and in bacteria,
its degree of expression is distributed in an unpredictable
manner. Hassen et al. (2000) reported that UV-C irradiated cells
(0.3 J/cm2) of Serratia marcescens, Acinetobacter baumanni,
and Enterobacter aerogenes were able to repair more than 5
Log10 cycles of viable cells after visible light illumination
(24 h), whereas P. aeruginosa, which showed the highest UV-
C resistance, was not able to photoreactivate. The photorepair
ability of different strains of enteropathogenic E. coli strains has
been widely studied, with great variability observed. For in-
stance, Tosa and Hirata (1999) observed that the maximum UV
dose required for 90 % UV-C inactivation of E. coli O26 with
photoreactivation (0.023 mW/cm2 at 360 nm for 4.6 h) was 2.2-
fold times higher than that without photoreactivation.
Besides the microbially specific response, photoreactivation
depends on the delivered UV dose, the UV irradiation source,
and the visible light illumination conditions. The extent of
photoreactivation is often inversely related to the applied UV-
C dose (Lindenauer and Darby 1994). Thus, applying suffi-
ciently high UV doses, photoreactivation can be drastically
reduced. The use of MP instead of LP lamps has been proposed
as another strategy to control photoreactivation. Some studies
have demonstrated that MP sources resulted in lower photore-
activation levels of E. coli than LP lamps had for the same
germicidal UV dose (up to 10 mJ/cm2) (Oguma et al. 2002;
Zimmer and Slawson 2002). Halmich and Gehr (2010) attrib-
uted this phenomenon to simultaneous exposure to UV-C light
Food Bioprocess Technol (2014) 7:1–20
and visible light (400–800 nm). On the contrary, other authors
have found similar degrees of E. coli photoreactivation for both
MP and LP lamps after treatments of 40 mJ/cm2 (Guo et al.
2009). Furthermore, photoreactivation has been observed after
microbial inactivation by the broad spectrum of PX lamps
(Maclean et al. 2008). Therefore, processing conditions that
avoid photoreactivation should be better addressed to establish
adequate operational parameters.
Regarding post-illumination conditions, photoreactivation
takes place above a certain visible light intensity threshold.
According to Halmich and Gehr (2010), at least 440 l × (0.065
mW/cm2) of visible light is needed to initiate E. coli photoreac-
tivation. Once this threshold is surpassed, the photorepair rate
increases with the visible light intensity (Tosa and Hirata 1999).
However, the maximum survival obtained after photoreactiva-
tion is independent of the intensity level (Lindenauer and Darby
1994; Kashimada et al. 1996), indicating that it is the illumina-
tion time which determines the final recovery value. This is
because the limiting factor in the photorepair mechanism is the
frequency of photolyase attachment to the CPDs (Gehr and
Wright 1998). The higher the intensity of visible light, the higher
the probability of photons reaching the photolyase enzyme.
Moreover, the emission spectrum of visible light sources also
affects the photorepair rate (Bohrerova and Linden 2007;
Maclean et al. 2008). However, by comparing photorepair rates
based on photorepair fluence calculations (weighted at 300–500
nm), Bohrerova and Linden (2007) demonstrated that these rates
were independent of the lamp type, but larger differences could
be found using time-based comparisons. In addition, the delay in
visible light exposure after UV treatment is also important
(Lindenauer and Darby 1994; Hallmich and Gehr 2010).
Delaying exposure to visible light for 3 h suppressed photore-
activation after relatively low UV-C doses (10 and 20 mJ/cm2)
(Hallmich and Gehr 2010). Overall, to compare the repair ability
of different microorganisms, post-illumination conditions after
UV treatment should be carefully optimized to attain the max-
imum expression of photorepair ability.
Environmental factors such as temperature, pH, and ionic
strength influence the rate of the photoreactivation process.
Temperature has little effect on bacterial photoreactivation,
but it occurs faster at higher temperatures (37 °C) than at
lower ones (4 °C) (Liltved and Landfald 1996). The effect of
salinity seems to be greater than that of temperature. The
binding affinity of the CPD photolyase decreases under low
ionic strength conditions, and consequently, photoreactivation
decreases (Chan and Killick 1995).
Although photoreactivation is important in water disinfec-
tion, in food processing, photorepair could not play such an
important role because foods are normally stored and
transported under dark conditions in containers. However, it
should be considered when UV-processed foods are likely to
be exposed to visible light.
15
Product Parameters
Other characteristics of the treatment media may change the
bactericidal efficacy of most food preservation technologies. In
general, the pH and water activity of the treatment media are
the most investigated factors. Several authors have reported
that the lethality of UV treatments is independent of pH
(Quintero-Ramos et al. 2004; Gayán et al. 2011). This is
logical because the key target of UV light is DNA, so it would
affect cell envelopes minimally. However, the effect of water
activity (aw) has barely been investigated. It has been demon-
strated that water activity does not alter the UV resistance of E.
coli or S. typhimurium in liquid medium between 0.96 and 0.99
(Gayán et al. 2011, 2012a). Similarly, the water activity of food
powder (black pepper and wheat flour) decontaminated by
PUV did not affect the inactivation of S. cerevisiae between
0.3 and 0.6 (Fine and Gervais 2004). From a practical point of
view, the absence of effects from pH or aw on bacterial UV
resistance is of extreme importance because it facilitates the
application of this technology to any food product indepen-
dently of these factors.
The most influential product characteristics in terms of the
lethal efficacy of UV technologies are the optical properties,
mainly the UV absorbance and the turbidity of the medium.
Color components, soluble compounds, and suspended solids
can absorb, reflect, and scatter the incidental light, reducing the
number of photons available for killing microorganisms
(Koutchma 2009). This can be observed by comparing UV
resistance data from Tables 2 and 3, which were obtained using
clear media and food, respectively. The absorption coefficient
(α) is considered a good indicator of UV penetration depth in
clear liquids, and several authors have reported a good rela-
tionship between α and UV lethal efficacy (Koutchma 2009;
Gayán et al. 2011). For instance, Gayán et al. (2011) demon-
strated a linear relationship between α and the Log10 of the
inactivation rate of E. coli: The inactivation rate decreased 10
times by increasing the absorption coefficient by 15.9 cm−1.
The negative impact of suspended solids on UV decontamina-
tion has been also reported, but its direct effect on UV lethality
is not so clear (Koutchma 2009). In any case, although the
optical properties of foods can affect microbial UV resistance
to a great extent, their effects on UV light's lethal effectiveness
are due to light intensity attenuation rather than to direct
biological effects.
Combination Processes
The limited microbial lethality of UV light in media with a
high absorption coefficient and turbidity, such as most liquid
foods, promotes the development of combined processes. UV
technology can be combined with conventional and other
16
nonthermal processes to enhance the lethal effects of UV light
on microorganisms. The lethality of combined treatments can
result from an additive or synergistic effect. Synergistic lethal
effects are preferable when designing combined processes
because they allow for obtaining a specific level of inactiva-
tion, reducing the energy input and treatment intensity. This
synergy may arise when applied inactivation strategies act on
the same vital target, increasing the chances of irreversible
damage, or when they act on different sites, causing sublethal
damage in several areas of the cells, enhancing their overall
lethal potential (Ross et al. 2003). The intelligent design of
combined treatments requires knowledge of the mechanisms
of inactivation for each technology to be applied. A synergistic
effect has been observed in combining UV light with mild
heat, chemical agents, and ionizing radiation (Gentner and
Werner 1978; Gayán et al. 2011). However, the combination
of UV light with other nonthermal technologies such as pulsed
electrical fields or ultrasounds for fruit juice hygienization has
resulted in additive inactivation effects (Gachovska et al. 2008;
Char et al. 2010).
When combining UV light with cooling or mild heating,
first of all, it is important to distinguish the changes in UV
microbial survivability due to biological effects from those
caused by variations in the efficiency of UV sources at differ-
ent temperatures. The optimum temperature of 254 nm radia-
tion produced by LP lamps is 40 °C, and then it drops off with
increased temperature (Koutchma 2009).
Besides the physical influence of temperature on UV le-
thality, reducing treatment temperature has been associated
with lower UV inactivation. For instance, Oteiza et al. (2010)
compared the UV-C lethal efficacy of E. coli O135:H7 strain
33/98 in orange juice at 4 and 20 °C. Results demonstrated
that the DUV value obtained at 4 °C (168 mJ/cm2) was greater
than at 20 °C (191 mJ/cm2). The higher UV microbial resis-
tance at lower temperatures could be explained by the minor
number of pyrimidine dimers formed in vivo and by changes
in the interactions between DNA and DNA-binding proteins,
which help to maintain the correct functional DNA structure
(Matallana-Surget et al. 2010).
Above 40 °C, the synergistic lethal improvement of UV-C
light when treatment temperature is increased by up to 50–60
°C has been reported in laboratory media and food matrices
(Gayán et al. 2011, 2012a, b). For instance, UV-C inactivation
(27.10 J/mL) of E. coli in orange juice increased synergisti-
cally from 0.6 Log10 cycles at 25 °C to more than 6 Log10
cycles at 55 °C. Heat inactivation at this temperature and for
the same treatment time was negligible (Gayán et al. 2012b).
The mechanism of the synergistic effect of the combined
UV light and mild heating treatments (UV-H treatments) re-
mains unclear. Our preliminary results demonstrated that the
synergistic lethal effect of UV-H treatment on E. coli resulted
from the inhibition of DNA excision repair due to membrane
fluidification caused by simultaneous heating (Gayán et al.
Food Bioprocess Technol (2014) 7:1–20
2013). In addition, we reported that the number of envelope-
injured cells was higher after the UV-H treatment than after
heating alone, indicating that the sensitization of cell envelopes
or inability of cells to repair these structures also occurs (Gayán
et al. 2012a).
UV light also exhibits synergistic interactions in combination
with various chemical agents. In practice, such combinations
have been introduced in water disinfection as advanced oxida-
tion processes (AOPs). AOPs are based on the utilization of
secondary oxidants such as hydroxyl radicals, released by UV
photolysis decomposition of a chemical disinfectant to improve
the UV germicidal effect and the oxidation of organic com-
pounds. Paracetic acid (PAA, 0.5–1.5 mg/L) in combination
with UV-C light (8–10 mJ/cm2) can improve lethal efficacy on
pathogen vegetative bacteria synergistically (Koivunen and
Heinonen-Tanski 2005). Koivunen and Heinonen-Tanski
(2005) observed 2.2 Log10 cycles of synergistic inactivation of
E. coli by combining 3 mg/L of PAA with a UV-C dose of 10 J/
cm2. Alternatively, the combination of ozone (3.4 mg min/L)
and UV-C light (14 mJ/cm2) showed a synergistic lethal effect
(2.5 Log10 cycles of inactivation) on B. subtilis spore inactiva-
tion (Jung et al. 2008). Other chemical agents that can enhance
UV-C lethal efficacy include TiO2 (Wu et al. 2011) and ethanol
(Ha and Ha 2010). In general, a simultaneous combination has
greater lethal synergism than sequential treatments, probably
due to increased radical formation, and this synergy increases
when either the UV level or the chemical dose is raised
(Koivunen and Heinonen-Tanski 2005; Jung et al. 2008).
Overall, the combination of UV light with oxidant agents allows
for reduced disinfectant doses or treatment times required for
water disinfection, thereby decreasing processing costs.
Combining UV-oxidant agents for food hygienization has
been less studied, but this has been proven to decontaminate
eggshells (Rodriguez-Romo and Yousef 2005), seafood (Ramos
et al. 2012), and fruit and vegetable surfaces (Fonseca and
Rushing 2006) without affecting food quality. For instance,
Rodriguez-Romo and Yousef (2005) demonstrated that the
combination of UV-C light (90–150 mJ/cm2) followed by ozone
(12–14 % for 1 min) resulted in synergistic inactivation of
Salmonella enteritidis by 4.6 Log10 units or more.
Although interesting results have been found by combining
UV light with physical and chemical agents, more research is
needed to establish effective combined processes for food
hygienization. For this purpose, it is essential to know the
action mechanism for each hurdle as well as the environmen-
tal, process, and microbial factors that influence microbial
inactivation and cell damage.
Conclusion
Nowadays, rising interest in the use of UV-based technologies
for food processing has prompted researchers to study the
Food Bioprocess Technol (2014) 7:1–20
lethal effect of these technologies on foodborne microbes. UV
light's ability to inactivate a wide range of microorganisms has
been extensively reported. However, little information on the
UV resistance of significant foodborne and spoilage bacteria is
available. Therefore, extending existing data is necessary to
identify key pathogens of concern in order to design UV
inactivation processes. The high variability in UV resistance
observed among strains of pathogenic species, which is even
broader than the interspecies and intergenera variability, should
be considered. The age of growth and the growth conditions
for bacteria may exert important effects on UV sensitivity, and
therefore, they should be standardized so microbial resistance
can be properly compared. In addition, knowledge of microbial
factors that contribute to the high resistance of UV-tolerant
microorganisms, such as chromosome condensation or DNA
repair efficiency, could be useful in creating strategies that
improve UV lethal efficacy, for instance, irradiating cells under
adverse conditions to impair DNA repair.
From a practical point of view, UV sensitivity is an intrinsic
characteristic of each microorganism. However, there are other
extrinsic microbial factors, processing conditions, and food
characteristics which also affect the UV resistance to some
extent. Knowing the influence of some of these factors on
UV survivability is crucial for efficient microbial control.
Discrepancies in the effect of sublethal stressors prior to UV
treatment must be evaluated in order to prevent adverse situa-
tions that might endanger food safety. At the same time, recov-
ery conditions strongly determine microorganisms' capacity to
repair UV-induced damage and survive. Of course, exposure to
visible light after UV processing must be completely avoided.
Furthermore, the ability of microorganisms in foods to perform
what is known as “dark repair” should be evaluated.
Finally, the possibility of designing combined treatments
based on UV light and other physical or chemical agents has
been addressed. Deeper knowledge of the mechanisms behind
UV inactivation and the functioning of damage repair pathways
can help researchers to design intelligent treatment combina-
tions. Thus, the simultaneous combination of UV light with
mild heating, oxidant agents, or cell membrane-fluidificant
compounds may result in successful inactivation treatments.
Acknowledgments This study has been carried out with financial support
from the Ministerio de Ciencia e Innovación de España, EU-FEDER
(CIT020000-2009-40) and the Departamento de Ciencia, Tecnología y
Universidad del Gobierno de Aragón. E. G. gratefully acknowledges the
financial support for her doctoral studies from the Ministerio de Educación y
Ciencia de España.
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