Trends in Food Science & Technology 90 (2019) 147–156

Contents lists available at ScienceDirect

Trends in Food Science & Technology

journal homepage: www.elsevier.com/locate/tifs

Review

Airborne contamination in the food industry: An update on monitoring and T

disinfection techniques of air
Fabio Masotti∗, Stefano Cattaneo, Milda Stuknytė, Ivano De Noni
Dipartimento di Scienze per gli Alimenti, la Nutrizione e l'Ambiente, Università degli Studi di Milano, Via G. Celoria 2, 20133, Milan, Italy

A R T I C LE I N FO A B S T R A C T

Keywords: Background: hygienic and safe production is a high priority in the food industry. During processing, food may be
Bioaerosol subjected to bio-contamination. Accordingly, preservation of overall quality by keeping a clean environment is a
Air monitoring goal to pursue. Among microbial vectors, air is considered a contributing factor to cross-contamination.
Chemical fogging Scope and approach: nowadays, in food plants emphasis is paid to the assessment of air bioload in view of
Gaseous ozonation
prevention of recontamination. Normally, air entering a processing plant is chilled and filtered to remove un-
UV irradiation
desired microorganisms from outside. Nevertheless, apart from clean-room environments, uncontrolled factors
(processes, personnel, structures, etc.) contribute to the release of microorganisms in indoor environments, re-
sulting in generation of bioaerosols highly variable within and among plants, and on a daily basis within the
same plant.
Key findings and conclusions: this review focuses on the relevance of bioaerosol monitoring in the food industry,
providing an update of air sampling techniques and methods of analysis in view to strengthen preventive hy-
gienic actions. Disinfection procedures to minimize microbial counts in the air as additional safeguard to the
standard chemical sanitation protocols are reviewed. Benefits and limitations of air treatment by chemical
fogging, ozonation, uv irradiation or cold plasma are outlined. Air bioload monitoring and the implementation of
subsequent air disinfection procedures are a feasible and a routinely exploitable strategy to satisfy hygienic
requirements in food plants. Further research is required to face technical challenges and optimize the feasibility
of some disinfection technologies for the real-world of food environments.

1. Microbial contamination of food: routes, vectors and factors and instruction in food hygiene matters in relation to the work activity.
limiting spreading Also exposure to contaminated surfaces has been identified as a major
source of food contamination (Otto et al., 2011). Both food-contact
Food contaminants are classified as extraneous substances of either (e.g., equipment, utensils, workbenches, conveyor belts) and no food-
physical, chemical or biological origin. Microorganisms may be re- contact surfaces (e.g., drains, utility pipes, maintenance equipment,
sponsible for outbreaks of food-related illnesses or food spoilage. In a structures, and areas away from production such as hallways, entrances
generic food facility, major routes of food recontamination by micro- and welfare facilities) can collect microorganisms and other debris from
organisms are via surface contact, via personnel or via the air (Fig. 1) employees, as well as from the air and other materials. These mutual
(den Aantrekker, Boom, Zwietering, & van Schothorst, 2003). Gen- interactions among above cited vectors can boost the microbial spread
erally, the contribution of the first two routes is prevailing, but the in a food facility (Fig. 1). In general, the low incidence and/or viability
importance of each means of contamination is also a function of the of pathogens in suspension in the air makes the route of air-to-food of
type of product or process. This review deals with items related to food low impact on foodborne diseases (Pérez-Rodriguez, Valero, Carrasco,
contamination by air route. Employees can transfer microorganisms García, & Zurera, 2008). Nonetheless, the recontamination by air is
both directly (from their body to the food product) and indirectly noteworthy for products such as beverages, refrigerated dairy and cu-
(transferring contamination from one area/surface to another) linary products and products with very low viable counts, such as dried
(Aarnisalo, 2007). In this context, the Annex II of the European Reg- infant formulae (Reij, den Aantrekker, & ILSI Europe Risk Analysis in
ulation No 852/2004 on food hygiene (EC, 2004) takes into con- Microbiology, 2004). In high-risk areas, for instance after the last heat
sideration the relevant role of employees, establishing their supervision treatment before filling and packaging, the food product (e.g.,

∗
Corresponding author.
E-mail address: [email protected] (F. Masotti).

https://doi.org/10.1016/j.tifs.2019.06.006
Received 11 December 2018; Received in revised form 18 March 2019; Accepted 11 June 2019
Available online 14 June 2019
0924-2244/ © 2019 Elsevier Ltd. All rights reserved.
F. Masotti, et al. Trends in Food Science & Technology 90 (2019) 147–156

Additional actions in the management of food processing such as proper

selection of ingredients, food storage conditions, plant maintenance and
air filtration are efficient tools in view of keeping or improving food
safety. The relative contribution of these factors is variable as a function
of the food sector.
Food hygiene is currently defined as measures and conditions ne-
cessary to control hazards and ensure the safety of food at all stages of
the chain (Codex Alimentarius, 2003; EC, 2004). It is realized through
established prerequisite programs, including good manufacturing
practices (GMP), good hygiene practices (GHP) and standard operating
procedures (SOP), which contribute to make hazard analysis critical
control point (HACCP) an effective system to control food safety (Byrne,
Lyng, Dunne, & Bolton, 2008; Varzakas, 2016). Even with the best
Fig. 1. Overview of major sources/vectors of microbial contamination and their control measures in place, a food product may still pose a risk to the
interactions in the food industry. consumer (den Aantrekker et al., 2003). Thus, all means to reduce or
prevent contamination and to improve the suitability for consumption
beverages) is susceptible to recontamination. In dairy production fa- are considered part of the hygiene concept. A proper management of air
cilities, spray drying and milling operations have been reported as a quality can mitigate the introduction of microorganisms throughout the
possible means of microbial transfer, making dissemination of patho- production stream of a food product. Each food production facility
gens through ventilation a probable event (Mullane, Whyte, Wall, should evaluate the presence of microorganisms in the site, sampling
Quinn, & Fanning, 2008). To counteract the risk of airborne bioconta- both surfaces and the air, through the implementation of an environ-
mination in the filling room, air filters should be changed on a regular mental monitoring program (EMP) necessary for the subsequent de-
basis, and a positive air pressure should be adopted (Lawlor, Schuman, velopment of a food safety plan (FPS) (Pleitner, 2018). The developed
Simpson, & Taormina, 2009). By modelling studies, den Aantrekker EMP allows to evaluate the effectiveness of the microbial controls in
et al. (2003) carried out a quantitative estimation of the probability of place. Such activity is pivotal in a well-run company.
product contamination via the air. Assuming settling velocities of mi- This review aims at highlighting the role of the airborne route in the
croorganisms under the influence of gravity only, the authors took into microbial spreading in the food industry. The scope is to provide an
consideration what-if scenarios to exemplify the determination of de- overview on both bioaerosol monitoring, including air sampling tech-
sign criteria to control a specified contamination level. As a conclusion, niques and methods of analysis, and on subsequent air disinfection
both the type of product and processing conditions strongly influence procedures as a proactive strategy in addition to routine sanitation
the contamination level. Comprehensive approaches to model factory practices. The items covered in this review are addressed to food safety
air movements have been described in literature and represent a con- aspects. Studies related to the field of occupational health are outside of
tribution of research to improve the understanding and tackling of the scope. The major target readers are food business operators who can
microbiological risks (Pérez-Rodriguez et al., 2008; Possas, Carrasco, perceive the potential advantages in terms of food safety arising from
García-Gimeno, & Valero, 2017). the implementation of environmental control protocols.
Other factors can contribute to microbial transfer to food, namely,
raw materials, ingredients, pests, water, processing conditions, packa- 2. What is a bioaerosol and why air monitoring is important?
ging material, transport vehicles, plant design, poor zoning, open
drains, as well as wet and dry cleaning operations by brushing, which The suspensions of microscopic solid or liquid particles in the air are
often result in the generation of bioaerosols in the form of water dro- defined as aerosols (Ferguson, Cumbrell, & Whitby, 2019). Those of
plets or dry dust (Ehavald, 2007; Marriott & Gravani, 2006). If cleaning major impact in the food sector are known as bioaerosols and consist of
and disinfection procedures are not performed in the correct manner, living substances with diameters up to 50 μm (Burfoot, 2016). These
residues of organic and inorganic soils could remain, and subsequently may include bacteria, mold spores and yeasts (Lee, 2011). Indeed, al-
food spoilage and pathogenic bacteria could create a suitable environ- though rarely documented, phage contamination can also occur
ment for biofilm development. In a wide range of food industries, through aerosolization (Verreault et al., 2011). Viruses can be found on
biofilms have become challenging (Marino, Maifreni, Baggio, & aerosol particles of various sizes, from the submicrometer range to tens
Innocente, 2018). In the topmost layers of the biofilm, chunks of the of micrometers in aerodynamic diameter. Virtually all microorganisms
extracellular polymeric substances, with the accompanying microbial present in bioaerosols are easily translocated by air currents, but their
population, can cross-contaminate other products, by the action of food reproduction is uncommon in the air due to the lack of moisture and
or liquid passing over the surface (Marriott & Gravani, 2006). To the nutrients. Despite the sensitiveness to environmental conditions, also
best of our knowledge, to date, detaching and air diffusion of above- food pathogens can survive in the air, for instance in association with
mentioned substances have not been reported. dust particles (Mullane, Whyte, Wall, Quinn, & Fanning, 2007). Ad-
Generally, epidemiological data on common contamination routes ditionally, contamination from airborne yeasts and molds can affect the
and sources are scarcely described in the literature (Reij, den quality and shelf life of a food product (Ehavald, 2007). The bioaerosol
Aantrekker, & ILSI Europe Risk Analisys in Microbiology Task Force, of the food industry is a mixture of many species of microorganisms
2004). Recent research in this area is focused to achieve greater insight including bacteria endospores and exospores (e.g., Bacillus, Clostridium),
into the mechanisms of microbial transfer and cross-contamination vegetative cells mainly of Gram positive bacteria (e.g., Micrococcus,
dynamics during food processing (Possas et al., 2017). Considering the Staphylococcus), molds (e.g., Penicillium, Cladosporium, Alternaria, Fu-
complexity of parameters involved in microbial transfer, it is apparent sarium) as well as yeasts (e.g., Saccharomyces, Torulaspora, Hansenias-
that only an integrated approach may be effective to prevent or mini- pora, Pichia) (Pérez-Martín, Seseña, Fernández-González, Arévalo, &
mize food contamination. Hygienic design of equipment/structures and Llanos Palop, 2014).
proper sanitation are factors limiting the microbial contamination in Aerosolized microorganisms may persist within droplets derived
full compliance with legislation (EC, 2004; EN 1672-2, 1997). Good from the aerosolization of water spraying/splashing during food pro-
hygiene practices include also personal hygiene, zone separation, pre- cessing or the sanitation process. In these cases, microorganisms grow
vention of cross-contamination, use of purified water (Gurnari, 2015). in a liquid medium, such as spilled product, rinse water or wastewater,
which subsequently becomes aerosolized. Microorganisms may also be

148
F. Masotti, et al. Trends in Food Science & Technology 90 (2019) 147–156

suspended as such in the air after dissipation or evaporation or as generic. The European regulation states the need to minimize airborne
“passengers” on solid dust particles (e.g., hair, clothing fiber, skin), contamination and to avoid mechanical airflow from a contaminated
which are dispersed in a food processing unit (Chang, Ting, & Horng, area to a clean area (EC, 2004). Guidances, intended to assist food
2019; Heo, Lim, Kee, & Lee, 2017). Microorganisms in the air may settle producers to meet the air quality and hygienic requirements of the food
on food products, equipment, containers and other food contact sur- manufacturing process, are available. The European Hygienic En-
faces during handling (Brandl et al., 2014). Any point at which the food gineering and Design Group (EHEDG) supported the European legisla-
product is exposed to air is a possible route for airborne contamination. tion producing a guideline focusing on air handling systems installed in
Combining the knowledge acquired under real situations in food fac- the food industry for air quality control (EHEDG, 2016).
tories and the use of computer models, Burfoot (2016) reported that the
smaller the particle suspended in the air the greater the flight time and 3. Bioaerosol monitoring: air sampling techniques and methods of
the distance it may travel. Indeed, the fate of airborne particles is quite analysis
complex and ruled by several mechanisms including: gravitational
settling, Brownian diffusion, inertial impaction, direct interception (by, The assessment of air microbial load in the food industry is per-
for example, van der Waal's forces) and electrostatic attraction (Da, formed through the sampling of a representative amount of air and its
Géhin, Havet, Ben Othmane, & Solliec, 2015). The combination of subsequent analysis. Quantification and identification of bioaerosols is
above-mentioned parameters influences the aerodynamic behavior of affected by several factors, such as the rate with which the result is
particles affecting the success of the air sampling. Generally, the air- required, the efficiency of sampling equipment, the ratio of total cell
borne particles most of interest in food environments are those con- counts versus viability of cells in the sample, the particle size range
taining bacteria with low-medium size (above 1 μm and below 20 μm) selected as well as the analysis methods (Dybwad, Skogan, & Blatny,
which can disperse easily around the generation area. By the way, 2014). Once the reasons for carrying out sampling have been defined,
aerosols in food plants have not been studied sufficiently to accurately the rate of relevance of above-mentioned parameters can be estab-
generalize particle-size distribution. Generally, in high-care areas less lished. The samplers should apply minimum stress during air collection
than 1% of particles in the air will settle, and most of them will be to reduce the impairment of the biological activity of the aerosol. In
removed by the filtration system. The contribution of airborne micro- addition, during air sampling, different environmental parameters can
organisms to food contamination has been addressed (Chang et al., cumulatively stress microorganisms affecting (through desiccation)
2019; Chen et al., 2019; Shale & Lues, 2007). Burfoot and Brown (2004) their viability. In long-term (> 30 min) sampling of bioaerosols, espe-
reported that the ratio of microorganisms to total particles may range cially for vegetative bacteria, the combination of controlled humidity
up to more than two orders of magnitude. For instance, these authors and refrigerated temperature of air sampler should provide viability
observed in different food factory environments that above-mentioned maintenance (Walls et al., 2017). The literature provides little in-
ratio was low (1–30,000) in periods of inactivity in a well-designed formation on the causative variables that lead to differing colony re-
production area, whereas it reached high levels (about 1–200) near to coveries (Wirtanen et al., 2002). Through years, to monitor air in a
employees during hand-washing and next to cleaning operations. To consistent way, performance measurements for air samplers have been
date, the awareness of the industry about the importance of the hy- reported using several efficiency terms, including aspiration-, sam-
gienic design, remarkably for the air handling system, is still low (Da pling-, recovery- and overall-efficiency (Dybwad et al., 2014). The
et al., 2015). Nonetheless, overemphasis on the role of air as a source of sampler efficiency is described also by factors such as the design of the
food contamination should be avoided. Burfoot, Whyte, Tinker, Hall, inlet, collection stage and choice of collection medium, which affect the
and Allen (2007) quantified the contribution of airborne microorgan- viability of microorganisms. Generally, the collection efficiency is ex-
isms to contamination of poultry carcasses undergoing processing in an pressed as the 50% aerodynamic cut-off diameter, Dae50 (μm), i.e. the
evisceration room. The use of ultra-clean air provided by a high-effi- particle size collected to 50% diameter. The proper choice of a sampler
ciency particulate air (HEPA) unit reduced total aerobic counts on with a Dae50 below the mean size of the particles being sampled is
horizontal settle plates by 68-fold. Differently, after measurement by crucial for efficient collection. The performance information supplied
sponging, the use of ultra-clean air had no effect on the counts on with commercially available samplers is often limited to collection ef-
carcasses. The latter resulted so heavily contaminated that the airborne ficiencies, but data on sampling stress are not always provided. Sum-
bacteria in the evisceration room represented less than 1% of total ming up, the evaluation of air microbial load is not a trivial task. It can
number of bacteria on carcasses. be performed through several sampling methods each with pros and
The food industry is aware that monitoring aerosols is becoming a cons (Table 1). Recently, Reponen (2017) reviewed the techniques of
must in standard quality-control practices. Generally, the primary focus air sampling of microorganisms in generic environments providing a list
is addressed to total viable microorganisms rather than total particle of commercially available bioaerosol samplers. Both passive (settle
counts. Air monitoring can be included as a part of an HACCP system in plates) and active (using a sampling device) air sampling techniques
the food industry (Beletsiotis, Ghikas, & Kalantzi, 2011). The role of can be adopted (Haig, Mackay, Walker, & Williams, 2016; Reponen,
bioaerosol monitoring consists in: 2017). The former approach consisting in the exposure of agar plates to
air for a certain period of time has been traditionally used. In this case,
- being the basic step for prevention; the collection is governed by gravitational force, which is related to the
- implementing a pro-active action to minimize cross-contamination particle mass. Settle plates technique is not quantitative, and in high
phenomena, which are major contributors in food-borne outbreaks; aerosol concentrations the uncountable numbers of colonies may re-
- complying with legal requirements or guidelines stating that the air present a problem. Active bioaerosol sampling exploits different col-
in food sector has to be controlled without specifying the metho- lection principles, such as impaction, impingement, cyclonic separa-
dology or minimum acceptable standards (Wray, 2011); tion, filtration, thermal or electrostatic precipitation. A large number of
- finding the potential source of new contamination whenever any commercial samplers is available on the market. Nevertheless, different
structural implementation has been introduced, and subsequently results are obtained from different equipment in the same place, at the
undertaking appropriate corrective measures; same time (Verreault, Moineau, & Duchaine, 2011). Properties and
- collecting epidemiological data, possibly with a view to set occu- critical factors affecting the use of air samplers have been recently re-
pational exposure limits (Wirtanen, Miettinen, Pahkala, Enbom, & viewed by Brown and Wray (2014). Data comparison is difficult be-
Vanne, 2002). cause the type of the device is reflected in the biodiversity of the
bioaerosol (Mbareche, Veillette, Bilodeau, & Duchaine, 2018). Dybwad
Information sources provided by the food legislator are quite et al. (2014) through a comparative evaluation of 9 different samplers

149
F. Masotti, et al. Trends in Food Science & Technology 90 (2019) 147–156

Sources: H. M. L. Lelieveld, M. A. Mostert, & J. Holah, 2005. Handbook of hygiene control in the food industry. Oxford, UK: Woodhead Publishing Limited; Ljungqvist & Reinmüller, 2007; Verreault et al., 2011; Reponen, (impactors, impingers, cyclones, electrostatic precipitators and filtra-
tion samplers) revealed significant differences in terms of cultivation-
based biological sampling efficiencies and PCR-/microscopy-based
Use in real food
physical sampling efficiencies as a function of the bioaerosol's stress–-
sensitivity and particle size. Typically, impaction is a common tech-
industry

++ nique for the collection of airborne viable particles (Miettinen, 2016).

++

++

+
In particular, there are two types of solid-surface impactors: slit sam-

–
plers and sieve samplers, the latter being preferred. In a sieve sampler
Selective for large air particles. Tendency to higher counts than other air the air is drawn through a large number of small, evenly spaced holes

Impractical in industrial use. Sterilization of the device after each use.

Qualitative method, based on collection by “fall out”. Biased to larger

drilled in a metal plate. Air particles impact on an agar surface located

below the perforated plate. The Andersen sampler, a cascade-sieve
impactor is likely the most-known device giving information on the size
distribution of the microbiological aerosol. Liquid-using impactors,
called impingers, are useful for sampling heavily contaminated air
thanks to the dilution of the liquid sample for the subsequent culture
growth analysis. Other instruments adopted in the food industry in-
clude centrifugal samplers based on cyclonic separation. In this case, air
is pulled into the sampling unit and pushed outside thus impacting on a
particles. Sensitive to air movements.

strip of nutrient agar. Such device is characterized by selectivity for

Possible stress by cell desiccation.

large particles, which are likely to include viable particles. For this
reasons the tendency is to exhibit higher counts than with other de-
Possible loss of survivability.

vices. A further type of active sampler, relying on filtration as a col-

lecting mechanism, is the filter system, which is recognized to be sui-
table for the subsequent enumeration of mold or bacterial spores.
Cost of device.

Airborne microorganisms can be collected also through electrostatic

In food sector.
No literature

precipitators following ionization and subsequent deposition in an

samplers.

electric field on a growth medium. The adoption of this technique re-

Cons

sulted more efficient than other methods (such as impingers) for sen-
sitive microbial strains e.g., Pseudomonas fluorescens (Miettinen, 2016).
Useful for collection of viruses or sensitive microbial strains. Compatible with analysis by
Multiple choice of devices (slit and sieves). Practical in industrial use. Information on size

Available as portable hand-held instrument. Practical in industrial use. Less cell stressing

Not expensive. Simple to operate. Suitable for enumeration of molds and bacterial spores.
Easy and cheap device to monitor generic air bioload. No cell stress by reduced viability.

Each of the above-mentioned devices has limitations that the user

should be aware of. To date, in the food industry settle plates and im-
pactors, being simple and practical, are the most used devices for
routine microbial air monitoring.
After collection, the air sample is analyzed through culture, mi-
croscopic, biochemical, immunological or molecular assays (Mbareche,
Brisebois, Veillette, & Duchaine, 2017; Reponen, Willeke, Grinshpun, &
Nevalainen, 2011). The choice of the analytical method relies on factors
including cost, time required, sensitivity, specificity and the sampling
method used. The selection is defined before air sampling is carried out.
Traditionally, in the food industry culture-based methods prevail for
Useful for heavily contaminated air environments.

enumerating the airborne microbial counts (Oppliger, 2014). Micro-

organisms collected by impaction are cultured directly, whereas fol-
lowing the use of filter systems the transfer to a culture medium is re-
quired. Usually, for surveys on the characterization of the airborne
distribution. Used to recover viruses.
Pros and cons of air sampling techniques available for the food industry.

microbiota the selection of general media is preferred, because it favors

the growth of a large diversity of species. The simultaneous isolation of
Used also to recover viruses.

polymerase chain reaction.

both bacteria and fungi is not satisfactory using only one culture
than impaction methods.

medium. In case of volumetric samplings, the concentration of culti-

vable airborne microorganisms is obtained by referring the colony
forming units (CFU) to the volume of air sampled. The limitation of
plate count method is that it reveals only a part of the microbial po-
++, frequent use; +, occasional use; –, not used.

pulation. Some bacteria may be in an eclipsed state defined as viable

Pros

but not cultivable (VBNC) as a response to stress conditions (Maukonen,

2007). Despite this disadvantage, plate count method is by far the gold
Air sampling

standard in food microbiology. In addition to culture technique, also

microscopic analysis is used to estimate the total number of micro-
Passive

Active

Active

Active

Active

Active

organisms in an air sample, allowing enumeration of both cultivable

and non-cultivable microorganisms. Direct microscopy is generally
employed to identify fungi, exploiting the morphological characteristics
Electrostatic precipitator

of spores. Phase-contrast microscopy allows to count bacterial en-

dospores due to their phase-bright appearance in contrast to darker
Cyclone separator

vegetative cells. Recently, investigations focused on health effects fol-

Settle plate

lowing exposure to harmful bioaerosols, led to a demand for accurate

Impinger
Impactor
Sampler

and reliable monitoring systems (Choi, Kang, & Jung, 2015). Molecular
Table 1

Filter
2017.

techniques such as polymerase chain reaction (PCR) amplification of

16 S rDNA, followed by its sequencing and DNA-DNA hybridization

150
F. Masotti, et al. Trends in Food Science & Technology 90 (2019) 147–156

allow to increase sensitivity and specificity, while decreasing the time of fungal contamination deriving from the outdoor environment. The
required for analysis (Stetzenbac, Buttner, & Cruz, 2004). Indeed, in the aerobiology of commercial dairy environments was investigated also by
food industry, the development of real-time continuous monitoring of Soldatou, Psoni, Tzanetakis, and Litopoulou-Tzanetaki (2006) through
microorganisms in the air would be important to verify the occurrence sedimentation technique and subsequent incubation. The authors iso-
of undesired trends that are not always revealed with periodic sam- lated mainly micrococci and bacilli in two cheese factories making Feta
plings. Through years, the quantitative PCR ((q)PCR) developed in the cheese. Physiological and biochemical activities of abovementioned
medical research area for assessing total or species-specific airborne microflora were investigated too. The air contaminants exhibited
bacterial load. Besides, the use of (q)PCR is more suitable than other acidifying and proteolytic activities potentially contributing to cheese
techniques for the analysis of air samples in the detection of phage ripening and flavor. More recently, Brandl et al. (2014) studied the
genome (Verreault et al., 2011). In this case, various sampling devices bioaerosol in different sites of milk powder and powdered infant for-
can be used to recover airborne viruses. Nevertheless, it is still chal- mula processing units of a dairy plant. As expected, due to the strict
lenging to study viral aerosols using metagenomics mainly due to hygienic requirements of these environments, numbers of cultivable
limited quantity of viruses in the air samples and due to the limited microorganisms were very low (< 100 CFU/m3 of air) during produc-
viral databases for viral metagenome library analysis (Behzad, tion in filling, bagging and final packaging zones in comparison with
Gojobori, & Mineta, 2015; Prussin, Marr, & Bibby, 2014). To date, the other industrial locations. Additionally, following measurements on
most common techniques to recover viruses are liquid and solid im- particle sizes of air, through handheld laser particle counters, the au-
pactors as well as filters. An extensive compilation of studies (mostly thors found a high correlation between total airborne particles in the
experimental in controlled chambers) on the recovery of viral particles size range 1–5 μm and numbers of CFU. The authors concluded on the
was carried out by Verreault et al. (2011) The (q)PCR technique is practical usefulness of a simple surveillance system based upon laser-
advantaged by the coupling to other molecular methods (like sequen- mediated counting of airborne particles occurring in a specified size
cing and DNA-DNA hybridization) to obtain information about the range. Simon and Duquenne (2014) referred on the airborne bioload,
species diversity (Oppliger, Charrière, Droz, & Rinsoz, 2008). The measured by an impactor sampler, in cheese-maturing cellars. Con-
sensitivity of (q)PCR is of different orders of magnitude higher than that centrations from 103 to 106 CFU/m3 and from 104 to 2 × 108 CFU/m3
of culture techniques. Moreover, it is able to amplify the DNA of VBNC were recorded for bacteria and fungi, respectively. Such levels resulted
cells. Nonetheless, given current available technologies, it is impossible from 1 up to 5 log10 cycles (brushing area) higher than those revealed in
to real-time monitor all the airborne biological agents and classify them points of the plant considered uncontaminated. The authors concluded
to the species level (Yao, 2018). To date, in the food industry, despite that throughout the process certain employees are exposed to high
the above discussed advantages, biochemical and molecular methods concentrations of airborne cultivable fungi.
are not applied as routine techniques to monitor indoor microbial air Few studies focused on the composition of the microbiota present in
quality. the air of wineries, in particular on yeasts, both beneficial and spoilage
ones (Ocón et al., 2013), and molds (Ocón et al., 2011). An in-depth
4. Levels of air contamination in commercial food processing study on the microbial ecology in the air of a winery was recently re-
plants viewed by Pérez-Martín et al. (2014).
Overall, above discussed investigations remark the large variability
The presence of microorganisms in the air of food facilities is pre- of microbial air counts in food commercial plants as a function of a
dominantly accidental and is highly variable or transient, generally range of factors, including the sector, the hygienic requirements of each
ranging from 10 to 10,000 CFU/m3 (Ehavald, 2007). Based on the as- zone of the plant, the design, as well as processing conditions. To date,
sumption that it is impossible to keep microbial counts at zero level, the legislator does not impose any restriction on the number of airborne
information on bioaerosol is important to evaluate the risk on both microorganisms being aware of the complexity of an ecosystem such as
product quality and/or shelf life and public health. the air in the food industry. Nonetheless, the European Community
In processing plants producing pork, poultry, beef and dairy pro- Board (European Collaborative Action, 1996), in the context of the
ducts, air has been recognized as a contributor to food contamination. provision of healthy and environmentally sustainable buildings laid
In particular, environments such as slaughterhouses are potentially down a report on indoor air quality and its impact on man. In this
critical, because animals are a microbial source of contamination. document, the air of generic indoor environments (private houses, non-
Prendergast, Daly, Sheridan, McDowell, and Blair (2004) investigated industrial workplaces and public buildings) was categorized in “very
the aerobiology of slaughter operations in two commercial beef abat- low” (< 50 CFU/m3), “low” (50–100 CFU/m3), “medium”
toirs. Although quantitatively different, both of them showed a similar (100–500 CFU/m3) and “high” (> 500 CFU/m3).
trend in counts within intraday processing, with lower levels before
slaughtering (about 1 log10 CFU/m3 of air). The authors observed dif- 5. Air handling
ferences in the aerial contamination among different sites in one
abattoir. In this case, total viable counts differed significantly The food environment is often wet and includes many sources of
(P < 0.001) ranging from 1.79 up to 3.47 log10 CFU/m3 of air in the aerosols contributing to microbial contamination, especially in critical
zone collecting washed carcass (“clean area”) and in the exsanguination areas where the products are exposed to air for long periods. Different
site (“dirty area”), respectively. This pattern was not observed in the physical mechanisms affect the movements of airborne particles re-
other abattoir due to the different building design, which allowed to sulting in a greater difficulty to control their movements. Generally,
effectively reducing the penetration of airborne contamination from proper implementation of air-handling equipment can ensure that a
“dirty” to “clean” areas. In addition to what has been already men- large part of the airborne particles does not come into contact with
tioned, Pearce, Sheridan, and Bolton (2006) in a pork slaughtering exposed foods. An approach to reduce air microbial load consists in the
plant enumerated about 1 log10 cycle decrease of aerobic mesophilic filtration of air entering a specific area. Besides filtration, also a
bacteria from the “wet” room (bleeding site) to the “clean” room heating, ventilation and air conditioning (HVAC) system is widely used.
(chilling site). The authors pointed out the role of animals as a source of This equipment allows the desired management of temperature and
air contamination. humidity of air as well as the flow direction and the pressurization
In a dairy plant, Beletsiotis et al. (2011) recovered as dominant within a specific area allowing to control airborne microorganisms. The
fungal genera Cladosporium spp., Penicillium spp. And yeasts. Due to the latter are not inactivated, but possibly accumulated on the filter surface
absence of an air filtration unit and the overlapping in the relative and can proliferate in case of high humidity (> 80%). Generally, an air
microbial air contamination, the authors ascribed the indoor presence flow of 1.5 m/s or greater is required to ensure maintenance of one-way

151
F. Masotti, et al. Trends in Food Science & Technology 90 (2019) 147–156

flow. Temperatures and relative humidity (likewise atmospheric gases, 7. Air disinfection by chemical fogging
light, irradiation and surrounding organic material) are environmental
factors associated with survival and growth of airborne microorganisms Fogging or aerosolization is the dispersion of a liquid in the form of
(Ijaz, Zargar, Wright, Rubino, & Sattar, 2016). Therefore, the control of fine mist in the air. Aerosolized disinfectants have been applied since
these factors is desirable. To remove the heat load imposed by the many years for therapeutic use in the healthcare sector (Otter, Yezli,
processing environment (processes and people) and to provide em- Perl, Barbut, & French, 2013). Subsequently, this technique has been
ployees with fresh air, 5–25 air changes per hour are considered suffi- implemented also in food factories for decontamination of products
cient. Proper ventilation removes also moisture released during pro- (fruits and vegetables) (Oh, Gray, Dougherty, & Kang, 2005) or disin-
cessing and prevents condensation and the subsequent mold growth on fection of surfaces in packaging or storage areas, process lines, cooling
surfaces. In addition, to prevent bioaerosol contamination within HVAC chambers (Holah et al., 1995). Fogging is also used to reduce the counts
systems, it is crucial to have a good understanding of the mechanisms of of airborne viable microorganisms deriving from low-care areas,
particle deposition and the subsequent fouling rate (Da et al., 2015). In people, structures, or formed as aerosols during cleaning procedures
food manufacturing facilities, the use of computational fluid dynamics (Burfoot, Hall, Brown, & Xu, 1999). The ultrafine droplet size of the dry
programs is a useful tool for prediction of airflow movements inside fog prevents it from easily falling onto surfaces, a desirable quality for
specific areas. This approach supports the correct placement of air area decontaminations (Krishnan et al., 2012).
ventilation systems enhancing good sanitary of food processing en- This technique has been also used quite widely by chilled food
vironments (Skåra & Rosnes, 2016). manufacturers, especially in high-care environments such as salad,
sandwich, ready meal and dairy processing. Typically, the process re-
quires at least 15–30 min for fog dispersion and proper chemical action.
6. Air disinfection Subsequently, to allow settling of suspended droplets, a period of
45–60 min is necessary to reenter the treated room. Various types of
In general, to inactivate environmental bioaerosols, different mi- delivery systems of the disinfectant solution in the air in the form of fine
crobial decontamination technologies have been investigated. These mist are available (Brown & Wray, 2014). Either a static purpose-built
include carbon nanotube filter, ion emissions, UV irradiation and system with strategically placed nozzles or, more commonly, a mobile
electrostatic field (Liang et al., 2012). In the air of a food facility, type unit can be adopted (Holah, 2011). Over the years, fogging automatic
and amounts of microorganisms can vary widely as a function of the site systems developed. The engineering of devices, in particular the type of
and on a day-to-day basis in the same environment (Masotti et al., nozzle, is of primary importance for the success of the treatment.
2019). To strengthen preventive measures against air bioload, in view Checking nozzles for clogging and gaskets for integrity are preliminary
of attaining the goal of providing a safe and a high quality product to steps to take before the disinfection treatment. Fogging is generally
the consumer, food business operators are interested in the adoption of categorized, on the base of droplet size, into atomization (or neb-
additional approaches other than regular sanitation procedures. In ulization) and aerosolization (Stanga, 2010). The former term is used
particular, chemical fogging, ozonation and UV irradiation of the air are when droplets have a diameter > 30 μm. These sizes result in shorter
major commercially available solutions. These techniques are currently settling times, undesirable moistened surfaces and reduced disinfecting
implemented in the pharmaceutical and clinical sectors, but far from activity. Typically, with aerosolization, droplets of disinfectant are no
being common in food processing environments. Each of these techni- wider than 5 μm. Small sizes (within the range 0.5–5 μm) characterize
ques is characterized by benefits and drawbacks to be properly eval- droplets with non-wetting surface, longer suspension times and an
uated for effective disinfection (Table 2). In the food industry a steady electric charge as a consequence of friction during the aerosolization.
growing interest is arising in these additional disinfection practices to Fogging for air disinfection of food environments is a scarcely stu-
minimize cross-contamination from the air, especially in critical areas died research topic (Bore & Langsrud, 2005). Burfoot et al. (1999) re-
(e.g., filling, packaging). One prerequisite for their effective im- ported that in the chilled food industry, fogs were most effective when
plementation is the application to closed environments. the diameter of droplets lied between 10 and 20 μm giving a uniform
coverage and a reasonable settling time (45 min). Up to 3 log10 cycle

Table 2
Pros and cons of disinfection techniques available in food industry for air treatment.
Sources: Burfoot et al., 1999; Marriott & Gravani, 2006; Pascual et al., 2007; Stanga, 2010; Krishnan et al., 2012; Cutler & Zimmerman, 2011; O’Donnell et al., 2012;
Christ et al., 2016; Zhou et al., 2016; Yang et al., 2018; Chen et al., 2019; Masotti et al., 2019.
Disinfection technique Pros Cons Use in food
industry

Air filtration and UV Disinfection efficacy of in-duct UV-C lamps. Energy consumption. Increase of temperature of air supply. Fungi ++
irradiation can escape UV radiation.
Chemical aerosolization Wide spectrum of efficacy against microorganisms. Time for aerosolization and chemical action. Sealing of treated +
Environmental friendliness (as a function of the agent used). environments. Controlled room re-entry, to avoid safety issues.
Dry aerosol. Equipment material compatibility.
Ozone gas Excellent antimicrobial activity. Production in situ. Health and safety issues in case of uncontrolled room re-entry. +
Immediate action. Auto-decomposition. Need of a gaseous ozone analyzer. Absence of personnel and food.
Lack of residues on food. Use of sealed environments. Corrosive to several soft metals and
rubber.
Cost of ozone generator.
UV irradiation Discrete disinfection efficacy. No use of chemicals. Health effects due to the production of ozone as a by-product. +
Synergistic effectiveness when in tandem with other Delivery of sufficient UV irradiation to large volumes of air.
technologies (e.g., photocatalysis, air filtration). Influence of environmental conditions.
Cold plasma Disinfection efficacy in air duct flow. Static purpose-built Health effects due to the production of ozone as a by-product. Cost –
system or mobile unit. of cold plasma tubes. No up-scale for commercial applications.
Lack of research data on air disinfection effectiveness in food
environments.

++, frequent use; +, occasional use; –, not used.

152
F. Masotti, et al. Trends in Food Science & Technology 90 (2019) 147–156

reduction was measured in air microbial counts as well as on upward- both to save water in comparison to the use of other biocides and to
facing surfaces, by using an active concentration of 2 mg/mL of a improve the quality of wastewaters, for instance by avoiding the pre-
quaternary ammonium formulation. Smaller droplets allowed a good sence of harmful chlorine compounds. Furthermore, ozone is generated
distribution, but the fog remained airborne for several hours, thus not in situ on demand without the need to store it. On the other hand, some
allowing the entering of personnel in the working area. Bagge-Ravn, disadvantages consist in the high capital cost (i.e., the corona discharge
Gardshodn, Gram, and Fonnesbech Vogel (2003) in the slicing area of a generator). Despite this, ozone treatment remains more cost-effective
salmon smokehouse evaluated the efficacy of peracetic acid-based than alternative treatment techniques.
fogging. After spread of a dense fog (mean droplet sizes of 15 μm) by a Most studies focused on the effectiveness of ozone in the aqueous
mobile unit, air was monitored by passive air sampling through settle phase (ozonated water) against foodborne microorganisms attached to
plates exposed for 2 h in different spots of the room. The authors ob- food contact surfaces or for food decontamination (Baumann, Martin, &
tained a significant improvement of air hygiene level (expressed in Feng, 2009; Brodowska et al., 2017; Cullen & Norton, 2012). Only few
terms of reduction of total aerobic counts). More recently, by test trials published reports are available on the use of gaseous ozone. In this case,
in dairy environments, Masotti et al. (2019) reported the effectiveness the disinfection treatment is carried out in confined spaces, for long
of hydrogen peroxide aerosolization in the inactivation of airborne times (1–4 h vs 1–10 min of ozonated water; Pascual et al., 2007) gen-
microorganisms. The mist dispenser produced particles with diameters erally overnight and in the absence of personnel. Ozone in the gaseous
of 5–15 μm of aerosolized hydrogen peroxide. Weekly-based air treat- phase presents safety issues to humans, being a powerful irritant to the
ments in cheese making and packaging rooms lasted 16 and 20 min, respiratory tract and a cellular poison that interferes with the ability of
respectively, and were followed by 20 min of settling time to allow the lungs to fight infectious agents (Marriott & Gravani, 2006). In the
aerosol decomposition. Following the post-treatment air sampling, United States, the Occupational Safety and Health Administration
microorganisms were almost absent during 5 weeks of investigation in (OSHA) recommends that ozone exposure must not be higher than
the packaging room (< 10 CFU/m3), whereas in the cheese making 0.1 ppm by volume (the equivalent of 0.2 mg/m3 of air) under normal
area only a slight number of bacteria (63 CFU/m3) and molds (39 CFU/ working conditions for 8 h daily, or 40 h a week without adverse effects.
m3) were enumerated. The occurrence of these residual molds (mainly Exposure to ozone at 0.1–1.0 ppm causes irritation to eyes, throat and
represented by Cladosporium herbarum, Penicillium spp. And Alternaria nose as well as headaches. High levels (from 1.0 ppm up to 100 ppm)
alternata) was ascribed to recontamination from outdoor air and fail- result in asthma-like symptoms (Pascual et al., 2007). Therefore, effi-
ures in the facility design. cient systems for the detection and destruction of residual ozone after
Overall, major output from the literature on fogging disinfection the air disinfection treatment speed up its decomposition and are rea-
outlined the facts that i) this technique should not be considered as a sonably required for the safety of employees. Foreseeing the potential
substitute of the regular cleaning and disinfection procedures; ii) fur- risks, a continuous ozone analyzer, triggering a general alarm as soon as
ther research is required to comprehensively evaluate the impact of the concentration of ozone exceeds 0.1 ppm in the atmosphere of the
parameters such as type of chemical, relative humidity and tempera- ozonation room, should be installed. The above-mentioned term
ture; iii) the success of the aerosolization is related to the design of the “safety” also refers to the equipment and instrumentation. Ozone may
treated area. interact with the equipment and all surfaces. Therefore, it is essential to
take into consideration only ozone-compatible materials.
8. Air disinfection by ozone In the dairy field, in particular in cheese ripening rooms, ozone gas
proved to be effective in reducing the viable numbers of mold spores in
Ozone (O3) is a gas acting as a strong oxidizing agent and biocide the air. Serra, Abrunhosa, Kozakiewicz, Venâncio, and Lima (2003)
(Marriott & Gravani, 2006). It has a broad-spectrum antimicrobial tested gaseous ozone treatments (overnight, during non-work time) for
power, being active against bacteria, fungi, viruses, protozoa and bac- 20 weeks in a closed ripening room of unspecified cheese types. Ozone
terial and fungal spores (Pascual, Llorca, & Canut, 2007). For this generated at a rate of 8 g/h for 12 h/d allowed obtaining a 10-fold re-
reason, ozone has been used for decades for water treatment. An ex- duction in the viable airborne mold loads to mean levels < 50 MPN/m3
tensive review on the principles of ozone treatment, the mechanism of of air. Differently, the treatment did not affect the number of mold
action and applications in the food industry has been recently published spores and hyphae on food contact surfaces, due to the short half-life of
(Brodowska, Nowak, & Śmigielski, 2017). In food processing environ- ozone. On this basis, according to the authors, gaseous ozone is useful
ments the most advanced germicidal applications include food surface to reduce the sedimentation of airborne molds on cheese surface during
hygiene, sanitation of food plant equipment, treatment of food plant ripening. Pinto, Schmidt, Raimundo, and Raihmer (2007), in the ri-
waste and reuse of waste water (Guzel-Seydim, Greene, & Seydim, pening room of extra-hard cheeses, carried out an environmental dis-
2004). Ozonation is performed after the cleaning step, because the infection program consisting in the discontinuous generation of 0.48 mg
germicidal activity is lost following its contact with residual organic of gaseous ozone per m3 of air. Following a 40-day trial, the authors
material such as food debris. Several organizations and countries ap- observed 1.5 log10 reduction of fungal viable counts in the air, mean-
proved the use of ozone as antimicrobial agent for direct contact with while a lower but significant reduction was measured on cheeses sur-
drinking water and for food decontamination, including vegetables, face (0.7 log10 cycles). More recently, Masotti et al. (2019), investigated
fish, meat, poultry and dairy products (Brodowska et al., 2017; Christ, the effectiveness of air ozonation in the packaging room of a dairy
Savi, & Scussel, 2016; Tiwari & Rice, 2012). In recent years, ozonation factory over a 5-week period to reduce air contamination. The treat-
has become more and more widely accepted as an eco-friendly “green” ment realized overnight 3 h/d and for 3 d per week meanly resulted in
technology (O'Donnell, Tiwari, Cullen, & Rice, 2012). An increasing the absence of microbial growth in 92% of air samplings, whereas the
interest for ozone application resulted in the opinion of the Italian remaining ones were characterized for bioload levels < 20 MPN/m3.
Ministry of Health (2010) endorsing the use of gaseous ozone for dis- The authors underlined the usefulness of a periodic air ozonation as a
infecting empty cheese ripening and storage facilities. Portable ozone practical solution to counteract unexpected spike levels of bioaerosol
generators are now available. They have discharge units and fans to due to uncontrolled factors.
create the ozone at variable concentrations and catalytic converters to In general, before installing an ozone generator, an ad-hoc tailored
decompose ozone to oxygen after the treatment. Benefits related to the study is recommended to take into consideration factors specific to any
use of ozone consist in the easy access to hidden sites, being in the processing environment. This approach can allow designing a safe and
gaseous state. It has also the advantage of the absence of by-products, as efficient program of air disinfection contributing to the implementation
it breaks down quickly into oxygen without leaving undesirable re- of food safety management.
sidues on either food or food contact surfaces. This technique allows

153
F. Masotti, et al. Trends in Food Science & Technology 90 (2019) 147–156

9. Air disinfection by UV radiation 1.5 log10 in airborne bacteria and molds was observed. In bakeries, UV
lamps are used on bread slicing equipment to minimize contamination
Ultraviolet light in the frequency range 100–280 nm, categorized as from airborne molds (Begum et al., 2009). Recently, Yang, Zhang,
UV-C, is an established means of disinfection. Radiation at short wa- Nunayon, Chan, and Lai (2018) investigated the performance of UV
velengths (approximately 254 nm) allows inactivating microorganisms irradiation through experiments evaluating exposure time, UV dose
such as bacteria, viruses, protozoa, molds, yeasts and algae. This en- received and bacteria susceptibility. The authors confirmed that the
vironmentally friendly technology is established to reduce microbial ventilation duct UV germicidal irradiation system would potentially
contamination in the public health field (hospitals, health care facil- provide a supplementary solution for improving indoor air quality
ities, public shelters) and the pharmaceutical industry (Lee, 2011). In within mechanical ventilated/air-conditioned environments. Despite
the food industry, UV-C irradiation is exploited to disinfect air, surfaces UV-C is an effective microbial inactivation means, a drawback limiting
of plant, packaging materials, water as well as fruit and vegetables its application is the production of ozone, a molecule of concern for its
during post-harvest storage (Begum, Hocking, & Miskelly, 2009). The healthy effects (Ryan, McCabe, Clements, Hernandez, & Miller, 2010).
germicidal action mechanism consists in damaging deoxyribonucleic
acid (DNA), thus rendering the microbes incapable of replicating 10. Air disinfection by cold plasma
(Kowalski, 2009). Microorganisms in the air are inactivated as a func-
tion of both the distance from the source of radiation and reflection. Air ionization is a decontamination technology primarily focused on
Lamps installed together with suitable coating materials (e.g., stainless liquids or surfaces (Arnold, Boothe, & Mitchell, 2004; Liang et al.,
steel and anodized aluminum) allow to reflect as much as 80% of the 2012). Recently, this technique turned into the spotlight for the appli-
emitted radiation (Stanga, 2010). Currently, UV-C lamps used in air cation in the food sector to reduce microbial contamination of food
disinfection applications are low-pressure mercury vapor lamps. In- (Lacombe et al., 2015; Misra & Jo, 2017). Cold plasma has been re-
novation challenges consist in: i) lamp technology to develop more cently investigated also for air sterilization (Liang et al., 2012; Zhou,
versatile and efficient lamps, ii) the use of nontoxic materials, in drivers Yang, Lai, & Huang, 2016). The principle of this technique consists in
and controls to adapt performance as a function of the need (e.g. oc- the passage of the air over an ionizing tube emitting high voltage dis-
cupied/unoccupied room) and iii) systems to warn in case of malfunc- charge (in-duct system) resulting in positively and negatively charged
tion (Miller, Linnes, & Luongo, 2013). UV lamps prove to be very useful ions, clusters of oxygen ions, oxygen-containing radicals, UV-C irra-
when coupled with high efficient air filters in air ducts and store rooms diation and a series of combined effects of these factors (Niemira, 2012;
for seasoning, chilling and drying when foods cannot be removed (e.g., Zhou et al., 2016). These reactive chemical species attract naturally
cheese, salami, Parma ham) (Stanga, 2010). UV energy is mainly ap- charged airborne micro-organisms, damaging their membranes, DNA
plied after air passage through the HVAC air-handling ductwork (also and/or proteins. In addition, high-voltage electrical discharges result in
called “in-duct” system) allowing an effective air microbial inactiva- the generation of ozone. Thus, monitoring schemes should be im-
tion. Bacteria, viruses and molds that either grow or pass through the plemented to avoid the presence of excess ozone concentration in the
air handling system are reduced. In the real world of food environ- treated room. Measures to remove the ozone should be evaluated if
ments, the irradiation at high intensities remains not accessible to required. For the scale up to commercial treatment levels an optimi-
personnel in the room. Lamp locations and air movement patterns zation and a more complete understanding of these chemical processes
within a room need to be considered for optimal disinfection. The in- is required. An additional aspect to take into account for practical
activation of microorganisms is dependent on several parameters, in- considerations is the cost of cold plasma tubes and the decrease in the
cluding: i) the dose of radiation received (measured in J/m2), which is emission of ion species with time (Lai, Cheung, Wong, & Li, 2016).
the product of intensity (measured in W/m2) and exposure duration The in-duct cold plasma system is very useful for disinfecting large
(measured in s); ii) the wavelength of received radiation and iii) the quantities of air as it passes through the HVAC system before its re-
microbial sensitivity to UV-C radiation (Reed, 2010). For instance, for circulation. Obviously, this will only be useful for disinfection of con-
90% inactivation of Aspergillus niger, A. flavus and Penicillium roqueforti taminated air through the duct, but not at the sources, i.e. inanimate
the required UV-C doses are 132, 60 and 13 J/m2, respectively (Begum environmental surfaces (Lai et al., 2016). Despite recent appearance on
et al., 2009). This species-dependent response is a function of the market of cold plasma disinfection units for in-duct applications (Zhou
composition of conidia, which can be either thin-walled and with light et al., 2016), the limitation of this technology is the early stage of de-
pigmentation or dark-pigmented due to melanin. The latter component velopment and the variety and complexity of the necessary equipment.
is photo-protective and increases the survival and longevity of fungal
spores, whereas non-melanin compounds are less defensive against UV- 11. Conclusions
C radiation (Kowalski, 2009). The susceptibility of airborne micro-
organisms is also a function of temperature and relative humidity. In the course of time, the safety of food gained a high priority, be-
There is a substantial lack of information on air-based UV constants. cause industry has been under pressure to deliver products minimally
Furthermore, environmental conditions are known to affect UV light. processed, more fresh in taste and appearance, with less preservatives
For instance, as relative humidity increases, UV light becomes less ef- and with prolonged shelf life. Thus, intervention strategies to control all
ficient (Cutler & Zimmerman, 2011). The delivery of the required UV vectors of food contamination should be pursued. Bioaerosols in a food
dose uniformly and consistently to large volumes of air is a significant facility may be potential contributors to food spoilage. Due to factory
challenge given the current state of the technology. To date the UV air movements, a complete environmental control is complex and al-
inactivation of bioaerosols is considered an added value in comparison most impossible. In the design of new factories, proper planning in
to the standard chemical sanitation protocol alone. locating air inlets, extracts, doorways and processing equipment is of
Most research studies on UV irradiation are dedicated to food de- utmost importance to optimize air movements. The periodic monitoring
contamination and water purification (Begum et al., 2009). Investiga- of microbial levels in the air is useful to identify potential sources of
tions on air as the target medium are scarce (Miller et al., 2013). contamination. Intervention should be taken to maintain a bioaerosol
Cundith, Kerth, Jones, McCaskey, and Kuhlers (2002) reported that the load consistent with the hygienic requirements of the food product.
use of wall-mounted germicidal air cleaning units, using a combination Through years, air disinfection techniques such as chemical aero-
of UV light and electrostatically polarized low-density media filter, solization, ozonation and UV irradiation evolved providing a feasible
proved to substantially reduce the risk of microbial contamination of and cost-effective solution for the decontamination of selected areas of
meat products in a small meat processing plant. Under the conditions the facility. Air decontamination can entail the benefit of reducing
described by the authors, after 18 h of filtration a reduction from 1 to microbial settling on frequently touched or food contact surfaces, thus

154
F. Masotti, et al. Trends in Food Science & Technology 90 (2019) 147–156

preventing the risk of microbial spread. Furthermore, the im- chemistry of pollutants and wastes (pp. 1–20). Berlin: Springer-Verlag.
plementation of a proactive approach based on scheduled air disinfec- Dybwad, M., Skogan, G., & Blatny, J. M. (2014). Comparative testing and evaluation of
nine different air samplers: End-to-end sampling efficiencies as specific performance
tion treatments would be an ancillary strategy, especially in case of measurements for bioaerosol applications. Aerosol Science and Technology, 48,
inadequate hygiene of structures. 282–295.
EC (2004). Regulation (EC) No 852/2004 of the European parliament and of the council
of 29 April 2004 on the hygiene of foodstuffs. Official Journal of the European Union, L,
References 139, 1–54.
Ehavald, H. (2007). Food process hygiene, effective cleaning and safety in the food in-
den Aantrekker, E. D., Boom, R. M., Zwietering, M. H., & van Schothorst, M. (2003). dustry. In G. Wirtanen, & S. Salo (Vol. Eds.), Microbial contaminants & contamination
Quantifying recontamination through factory environments - a review. International routes in food industry. VTT Publication: Vol. 248, (pp. 129–144). Espoo, Finland:
Journal of Food Microbiology, 80, 117–130. Technical Research Centre of Finland (VTT).
Aarnisalo, K. (2007). Effect of maintenance routines in food processing on production EHEDG (2016). Document 47 - guidelines on air handling systems in the food industry. Air
hygiene. In G. Wirtanen, & S. Salo (Vol. Eds.), Microbial contaminants & contamination quality control for building ventilation.
routes in food industry. VTT Publication: Vol. 248, (pp. 36–38). Espoo, Finland: EN (1997). EN 1672-2. Food processing machinery - basic concepts - Part 2: Hygienic
Technical Research Centre of Finland (VTT). Requirements. Brussels, Belgium: European Committee for Standardization.
Alimentarius, C. (2003). Recommended international code of practice. General principles of European Collaborative Action (1996). Environment and quality of life. Report No. 12.
food hygiene CAC/RCP 1–1969, rev. 4–2003. Washington, DC: Codex Alimentarius Biological particles in indoor environmentsLuxembourg: Commission of the European
Commission. Communities.
Arnold, J. W., Boothe, D. H., & Mitchell, B. W. (2004). Use of negative air ionization for Ferguson, R., Cumbrell, A. J., & Whitby, C. (2019). Bioaerosol biomonitoring: Sampling
reducing bacterial pathogens and spores on stainless steel surfaces. The Journal of optimization for molecular microbial ecology. Molecular Ecology Resources. https://
Applied Poultry Research, 13, 200–206. doi.org/10.1111/1755-0998.13002 available at:.
Bagge-Ravn, D., Gardshodn, K., Gram, L., & Fonnesbech Vogel, B. (2003). Comparison of Gurnari, G. (2015). The reduction of microbial spreading: Little details, great effects. In G.
sodium hypochlorite–based foam and peroxyacetic acid–based fog sanitizing proce- Gurnari (Ed.). Safety protocols in the food industry and engineering concerns (pp. 19–30).
dures in a salmon smokehouse: Survival of the general microflora and Listeria London, UK: Springer-Verlag.
monocytogenes. Journal of Food Protection, 66, 592–598. Guzel-Seydim, Z. B., Greene, A. K., & Seydim, A. C. (2004). Use of ozone in the food
Baumann, A. R., Martin, S. E., & Feng, H. (2009). Removal of Listeria monocytogenes industry. Lebensmittel-Wissenschaft und-Technologie, 37, 453–460.
biofilms from stainless steel by use of ultrasound and ozone. Journal of Food Haig, C. W., Mackay, W. G., Walker, J. T., & Williams, C. (2016). Bioaerosol sampling:
Protection, 72, 1306–1309. Sampling mechanisms, bioefficiency and field studies. Journal of Hospital Infection,
Begum, M., Hocking, A. D., & Miskelly, D. (2009). Inactivation of food spoilage fungi by 93, 242–255.
ultra violet (UVC) radiation. International Journal of Food Microbiology, 129, 74–77. Heo, K. J., Lim, C. E., Kee, H. B., & Lee, B. U. (2017). Effects of human activities on
Behzad, H., Gojobori, T., & Mineta, K. (2015). Challenges and opportunities of airborne concentrations of culturable bioaerosols in indoor air environments. Journal of
metagenomics. Genome Biology and Evolution, 7, 1216–1226. Aerosol Science, 104, 58–65.
Beletsiotis, E., Ghikas, D., & Kalantzi, K. (2011). Incorporation of microbiological and Holah, J. (2011). Combating contamination with whole room disinfection. International
molecular methods in HACCP monitoring scheme of molds and yeasts in a Greek Food Hygiene, 21, 7–9.
dairy plant: A case study. Procedia Food Science, 1, 1051–1059. Holah, J. T., Rogers, S. J., Holder, J., Hall, K. E., Taylor, J., & Brown, K. L. (1995). The
Bore, E., & Langsrud, S. (2005). Characterization of micro-organisms isolated from dairy evaluation of air disinfection systems. CCFRA R&D Report No. 13Gloucestershire, UK:
industry after cleaning and fogging disinfection with alkyl amine and peracetic acid. Campden and Chorleywood Food Research Association.
Journal of Applied Microbiology, 98, 96–105. Ijaz, M. K., Zargar, B., Wright, K. E., Rubino, J. R., & Sattar, S. A. (2016). Generic aspects
Brandl, H., Fricker-Feer, C., Ziegler, D., Mandal, J., Stephan, R., & Lehner, A. (2014). of the airborne spread of human pathogens indoors and emerging air decontamina-
Distribution and identification of culturable airborne microorganisms in a Swiss milk tion technologies. American Journal of Infection Control, 4, S109–S120.
processing facility. Journal of Dairy Science, 97, 240–246. Italian Ministry of Health (2010). Opinion of the National Food Safety Committee on ozone
Brodowska, A. J., Nowak, A., & Śmigielski, K. (2017). Ozone in the food industry: treatment of air in cheese ripening rooms (In Italian). Available at: http://www.salute.
Principles of ozone treatment, mechanism of action, and applications: An overview. gov.it/imgs/C_17_pubblicazioni_1514_allegato.pdf (accessed December 2018) .
Critical Reviews in Food Science and Nutrition, 58, 2176–2201. Kowalski, W. (2009). Ultraviolet germicidal irradiation handbook. UVGI for air and surface
Brown, K. L., & Wray, S. (2014). Control of airborne contamination in food processing. In disinfection. Berlin: Springer-Verlag.
H. L. M. Lelieveld, J. Holah, & D. Napper (Eds.). Hygiene in food processing: Principles Krishnan, J., Fey, G., Stansfield, C., Landry, L., Nguy, H., Klassen, S., et al. (2012).
and practice (pp. 174–199). New Delhi: Woodhead Publishing. Evaluation of a dry fogging system for laboratory decontamination. Applied Biosafety,
Burfoot, D. (2016). Aerosols as a contamination risk. In H. M. L. Lelieveld, J. Holah, & D. 17, 132–141.
Gabrić (Eds.). Handbook of hygiene control in the food industry (pp. 81–87). Oxford, UK: Lacombe, A., Niemira, B. A., Gurtler, J. B., Fan, X., Sites, J., Boyd, G., et al. (2015).
Woodhead Publishing Limited. Atmospheric cold plasma inactivation of aerobic microorganisms on blueberries and
Burfoot, D., & Brown, K. L. (2004). A relationship between the airborne concentration of effects on quality attributes. Food Microbiology, 46, 479–484.
particles and organisms in chilled food factories. Paper 9 on CD ROM proceedings of the Lai, A. C. K., Cheung, A. C. T., Wong, M. M. L., & Li, W. S. (2016). Evaluation of cold
international conference on engineering and food, ICEF9, 7–11 march 2004, montpellier, plasma inactivation efficacy against different airborne bacteria in ventilation duct
France. flow. Building and Environment, 98, 39–46.
Burfoot, D., Hall, K., Brown, K., & Xu, Y. (1999). Fogging for the disinfection of food Lawlor, K. A., Schuman, J. D., Simpson, P. G., & Taormina, P. J. (2009). Microbiological
processing factories and equipment. Trends in Food Science & Technology, 10, spoilage of beverages. In W. H. Sperber, & M. P. Doyle (Eds.). Compendium of the
205–210. microbiological spoilage of foods and beverages (pp. 245–284). New York: Springer.
Burfoot, D., Whyte, R. T., Tinker, D. B., Hall, K., & Allen, V. M. (2007). A novel method for Lee, B. U. (2011). Life comes from the air: A short review on bioaerosol control. Aerosol
assessing the role of air in the microbiological contamination of poultry carcasses. and Air Quality Research, 11, 921–927.
International Journal of Food Microbiology, 115, 48–52. Liang, Y., Wu, Y., Sun, K., Chen, Q., Shen, F., Zhang, J., et al. (2012). Rapid inactivation of
Byrne, B., Lyng, J., Dunne, G., & Bolton, D. J. (2008). An assessment of the microbial biological species in the air using atmospheric pressure nonthermal plasma.
quality of the air within a pork processing plant. Food Control, 19, 915–920. Environmental Science & Technology, 46, 3360–3368.
Chang, C.-W., Ting, Y.-T., & Horng, Y.-J. (2019). Collection efficiency of liquid-based Marino, M., Maifreni, M., Baggio, A., & Innocente, N. (2018). Inactivation of foodborne
samplers for fungi in indoor air. Indoor Air, 00, 1–10. bacteria biofilms by aqueous and gaseous ozone. Frontiers in Microbiology, 9, 2024.
Chen, Y.-C., Liao, C.-H., Shen, W.-T., Su, C., Wu, Y.-C., Tsai, M.-H., et al. (2019). Effective https://doi.org/10.3389/fmicb.2018.02024.
disinfection of airborne microbial contamination in hospital wards using a zero-va- Marriott, N. G., & Gravani, R. B. (2006). Principles of food sanitation (5th ed.). New York:
lent nano-silver/TiO2-chitosan composite. Indoor Air, 00, 1–11. Springer.
Choi, J., Kang, M., & Jung, J. H. (2015). Integrated micro-optofluidic platform for real- Masotti, F., Vallone, L., Ranzini, S., Silvetti, T., Morandi, S., & Brasca, M. (2019).
time detection of airborne microorganisms. Scientific Reports, 5, 1–10. Effectiveness of air disinfection by ozonation or hydrogen peroxide aerosolization in
Christ, D., Savi, G. D., & Scussel, V. M. (2016). Effectiveness of ozone gas in raw and dairy environments. Food Control, 97, 32–38.
processed food for fungi and mycotossin decontamination. Journal of Chemical, Maukonen, J. (2007). Molecular techniques and microscopy in bacterial detection and
Biological and Physical Sciences, 6, 326–348. typing. In G. Wirtanen, & S. Salo (Vol. Eds.), Microbial contaminants & contamination
Cullen, P. J., & Norton, T. (2012). Ozone sanitisation in the food industry. In C. O'Donnell, routes in food industry. VTT Publication: Vol. 248, (pp. 46–50). Espoo, Finland:
B. K. Tiwari, P. J. Cullen, & R. G. Rice (Eds.). Ozone in food processing (pp. 163–176). Technical Research Centre of Finland (VTT).
Oxford: Wiley-Blackwell. Mbareche, H., Brisebois, E., Veillette, M., & Duchaine, C. (2017). Bioaerosol sampling and
Cundith, C. J., Kerth, C. R., Jones, W. R., McCaskey, T. A., & Kuhlers, D. L. (2002). Air- detection methods based on molecular approaches: No pain no gain. The Science of the
cleaning system effectiveness for control of airborne microbes in a meat-processing Total Environment, 599–600, 2095–2104.
plant. Journal of Food Science, 67, 1170–1174. Mbareche, H., Veillette, M., Bilodeau, G. J., & Duchaine, C. (2018). Bioaerosol sampler
Cutler, T. D., & Zimmerman, J. J. (2011). Ultraviolet irradiation and the mechanisms choice should consider efficiency and ability of samplers to cover microbial diversity.
underlying its inactivation of infectious agents. Animal Health Research Reviews, 12, Applied and Environmental Microbiology. https://doi.org/10.1128/AEM.01589-18.
15–23. Miettinen, H. (2016). Air sampling. In H. M. L. Lelieveld, J. Holah, & D. Gabrić (Eds.).
Da, G., Géhin, E., Havet, H., Ben Othmane, M., & Solliec, C. (2015). Preventing indoor Handbook of hygiene control in the food industry (pp. 697–709). Oxford, UK: Woodhead
bioaerosol contamination in food processing environments and HVAC systems: Publishing.
Assessment of particle deposition for hygienic design purposes. In E. Jiménez, B. Miller, S. L., Linnes, J., & Luongo, J. (2013). Ultraviolet germicidal irradiation: Future
Cabanas, & G. Lefebvre (Eds.). Environment, energy and climate change I: Environmental directions for air disinfection and building applications. Photochemistry and

155
F. Masotti, et al. Trends in Food Science & Technology 90 (2019) 147–156

Photobiology, 89, 777–781. Reed, N. G. (2010). The history of ultraviolet germicidal irradiation for air disinfection.
Misra, N. N., & Jo, C. (2017). Applications of cold plasma technology for microbiological Public Health Reports, 125, 15–27.
safety in meat industry. Trends in Food Science & Technology, 64, 74–86. Reij, M. W., den Aantrekker, W. D., & ILSI Europe Risk Analisys in Microbiology Task
Mullane, N., Healy, B., Meade, J., Whyte, P., Wall, P. G., & Fanning, S. (2008). Force (2004). Recontamination as a source of pathogens in processed foods.
Dissemination of Cronobacter spp. (Enterobacter sakazakii) in a powdered milk protein International Journal of Food Microbiology, 91, 1–11.
manufacturing facility. Applied and Environmental Microbiology, 74, 5913–5917. Reponen, T. (2017). Sampling for microbial determination. In C. Viegas, S. Viegas, A.
Mullane, N. R., Whyte, P., Wall, P. G., Quinn, T., & Fanning, S. (2007). Application of Gomes, M. Tӓubel, & R. Sabino (Eds.). Exposure to microbial agents in indoor and oc-
pulsed-field gel electrophoresis to characterise and trace the prevalence of cupational environments (pp. 85–96). Cham, Switzerland: Springer.
Enterobacter sakazakii in an infant formula processing facility. International Journal of Reponen, T., Willeke, K., Grinshpun, S., & Nevalainen, A. (2011). Biological particle
Food Microbiology, 116, 73–81. sampling. In P. Kulkarni, P. Baron, & K. Willeke (Eds.). Aerosol measurement, princi-
Niemira, B. A. (2012). Cold plasma decontamination of foods. Annual Review of Food ples, techniques, and applications (pp. 549–570). (3rd ed.). San Francisco, CA: Wiley.
Science and Technology, 3, 125–142. Ryan, K., McCabe, K., Clements, N., Hernandez, M., & Miller, S. L. K. (2010). Inactivation
Ocón, E., Garijo, P., Sanz, S., Olarte, C., López, R., Santamaría, P., et al. (2013). Analysis of airborne microorganisms using novel ultraviolet radiation sources in reflective
of airborne yeasts in one winery over a period of one year. Food Control, 30, 585–589. flow-through control devices. Aerosol Science and Technology, 44, 541–550.
Ocón, E., Gutiérrez, A. R., Garijo, P., Santamaría, P., López, R., Olarte, C., et al. (2011). Serra, R., Abrunhosa, L., Kozakiewicz, Z., Venâncio, A., & Lima, N. (2003). Use of ozone
Factors of influence in the distribution of mold in the air in a wine cellar. Journal of to reduce molds in a cheese ripening room. Journal of Food Protection, 66, 2355–2358.
Food Science, 76, 169–174. Shale, K., & Lues, J. F. R. (2007). The etiology of bioaerosols in food environments. Food
Oh, S.-W., Gray, P. M., Dougherty, R. H., & Kang, D. H. (2005). Aerosolization as novel Reviews International, 23, 73–90.
sanitizer delivery system to reduce food-borne pathogens. Letters in Applied Simon, X., & Duquenne, P. (2014). Assessment of workers' exposure to bioaerosols in a
Microbiology, 41, 56–60. French cheese factory. Annals of Occupational Hygiene, 58, 677–692.
Oppliger, A. (2014). Advancing the science of bioaerosol exposure assessment. Annals of Skåra, T., & Rosnes, J. T. (2016). Emerging methods and principles in food contact surface
Occupational Hygiene, 58, 661–663. decontamination/prevention. In C. E. Leadley (Ed.). Innovation and future trends in
Oppliger, A., Charrière, N., Droz, P.-O., & Rinsoz, T. (2008). Exposure to bioaerosols in food manufacturing and supply chain technologies (pp. 151–172). Cambridge:
poultry houses at different stages of fattening; use of real-time PCR for airborne Woodhead Publishing.
bacterial quantification. Annals of Occupational Hygiene, 52, 405–412. Soldatou, H., Psoni, L., Tzanetakis, N., & Litopoulou-Tzanetaki, E. (2006). Populations,
Otter, J. A., Yezli, S., Perl, T. M., Barbut, F., & French, G. L. (2013). The role of ‘no-touch’ types and biochemical activities of aerobic bacteria and lactic acid bacteria from the
automated room disinfection systems in infection prevention and control. Journal of air of cheese factories. International Journal of Dairy Technology, 59, 2000–2008.
Hospital Infection, 83, 1–13. Stanga, M. (2010). Sanitation: Cleaning and disinfection in the food industry. Weinheim:
Otto, C., Zahn, S., Rost, F., Zahn, P., Jaros, D., & Rohm, H. (2011). Physical methods for Wiley-VCH Verlag.
cleaning and disinfection of surfaces. Food Engineering Reviews, 3, 171–188. Stetzenbach, L. D., Buttner, M. P., & Cruz, P. (2004). Detection and enumeration of air-
O'Donnell, C., Tiwari, B. K., Cullen, P. J., & Rice, R. G. (2012). Status and trends of ozone borne biocontaminants. Current Opinion in Biotechnology, 15, 170–174.
in food processing. In C. O'Donnell, B. K. Tiwari, P. J. Cullen, & R. G. Rice (Eds.). Tiwari, B. K., & Rice, R. G. (2012). Regulatory and legislative issues. In C. O'Donnell, B. K.
Ozone in food processing (pp. 1–6). Oxford: Wiley-Blackwell. Tiwari, P. J. Cullen, & R. G. Rice (Eds.). Ozone in food processing (pp. 7–17). Oxford:
Pascual, A., Llorca, I., & Canut, A. (2007). Use of ozone in food industries for reducing the Wiley-Blackwell.
environmental impact of cleaning and disinfection activities. Trends in Food Science & Varzakas, T. (2016). Hygiene and food sanitation. In T. Varzakas, & C. Tzia (Eds.).
Technology, 18, S29–S35. Handbook of food processing food safety, quality, and manufacturing processes (pp. 73–
Pearce, R. A., Sheridan, J. J., & Bolton, D. J. (2006). Distribution of airborne micro- 104). New York: CRC Press.
organisms in commercial pork slaughter processes. International Journal of Food Verreault, D., Gendron, L., Rousseau, G. M., Veillette, M., Massé, D., Lindsley, W. G., et al.
Microbiology, 107, 186–191. (2011a). Detection of airborne lactococcal bacteriophages in cheese manufacturing
Pérez-Martín, F., Seseña, S., Fernández-González, M., Arévalo, M., & Llanos Palop, M. plants. Applied and Environmental Microbiology, 77, 491–497.
(2014). Microbial communities in air and wine of a winery at two consecutive vin- Verreault, D., Moineau, S., & Duchaine, C. (2011b). Methods for sampling of airborne
tages. International Journal of Food Microbiology, 190, 44–53. viruses. Microbiology and Molecular Biology Reviews, 72, 413–444.
Pérez-Rodriguez, F., Valero, A., Carrasco, F., García, R. M., & Zurera, G. (2008). Walls, H. J., Kim, J. H., Yaga, R. W., Harvey, L. A., Haines, L. G., Ensor, D. S., et al. (2017).
Understanding and modelling bacterial transfer to foods: A review. Trends in Food Long-term viable bioaerosol sampling using a temperature- and humidity-controlled
Science & Technology, 19, 131–144. filtration apparatus, a laboratory investigation using culturable E. coli. Aerosol Science
Pinto, A. T., Schmidt, V., Raimundo, S. A., & Raihmer, F. (2007). Moulds control by and Technology, 51, 576–586.
ozonization in ripening cheese room (In Brasilian). Acta Scientiae Veterinariae, 35, Wirtanen, G., Miettinen, H., Pahkala, S., Enbom, S., & Vanne, L. (2002). Clean air solutions
333–337. in food processing. VTT Publication 482. Espoo, Finland: Technical Research Centre of
Pleitner, A. (2018). Air quality in production facilities. Food safety net services. Post available Finland (VTT).
at: http://fsns.com/news/air-quality-production-facilities (accessed December Wray, S. (2011). Managing airflow and air filtration to improve hygiene in food factories.
2018) . In J. Holah, & H. L. M. Lelieveld (Eds.). Hygienic design in food factories (pp. 249–268).
Possas, A., Carrasco, E., García-Gimeno, R. M., & Valero, A. (2017). Models of microbial London: Woodhead Publishing.
cross-contamination dynamics. Current Opinions in Food Science, 14, 43–49. Yang, Y., Zhang, H., Nunayon, S. S., Chan, V., & Lai, A. C. K. (2018). Disinfection efficacy
Prendergast, D. M., Daly, D. J., Sheridan, J. J., McDowell, D. A., & Blair, I. S. (2004). The of ultraviolet germicidal irradiation on airborne bacteria in ventilation ducts. Indoor
effect of abattoir design on aerial contamination levels and the relationship between Air, 28, 806–817.
aerial and carcass contamination levels in two Irish beef abattoirs. Food Microbiology, Yao, M. (2018). Bioaerosol: A bridge and opportunity for many scientific research fields.
21, 589–596. Journal of Aerosol Science, 115, 108–112.
Prussin, A. J., Marr, L. C., & Bibby, K. J. (2014). Challenges of studying viral aerosol Zhou, P., Yang, Y., Lai, A. C. K., & Huang, G. (2016). Inactivation of airborne bacteria by
metagenomics and communities in comparison with bacterial and fungal aerosols. cold plasma in air duct flow. Building and Environment, 106, 120–130.
FEMS Microbiology Letters, 357, 1–9.

156