1035

Journal of Food Protection, Vol. 81, No. 6, 2018, Pages 1035–1040

doi:10.4315/0362-028X.JFP-18-031
Copyright Ó, International Association for Food Protection

Mini-Review

Fungal Spoilage in Food Processing

ABIGAIL B. SNYDER1* AND RANDY W. WOROBO2

1Department of Extension, The Ohio State University, 1680 Madison Avenue, Wooster, Ohio 44691; and 2Department of Food Science, Cornell University,
411 Tower Road, Ithaca, New York 14853, USA

MS 18-031: Received 18 January 2018/Accepted 12 February 2018/Published Online 16 May 2018

ABSTRACT
Food processing, packaging, and formulation strategies are often specifically designed to inhibit or control microbial growth
to prevent spoilage. Some of the most restrictive strategies rely solely or on combinations of pH reduction, preservatives, water
activity limitation, control of oxygen tension, thermal processing, and hermetic packaging. In concert, these strategies are used to
inactivate potential spoilage microorganisms or inhibit their growth. However, for select microbes that can overcome these
controls, the lack of competition from additional background microbiota helps facilitate their propagation.
Key words: Food processing; Fungi; Quality control; Spoilage

Fungi as a group are some of the most resilient spoilage disease, its economic impact, and the prevalence of specific
microorganisms and are capable of overcoming the control illnesses associated pathogenic microorganisms.
strategies utilized by the food industry. Various fungal Recent and persistent examples of microbial food
propagules are rapidly dispersed by water and air, survive spoilage recalls and product withdrawals, and emerging
under extreme conditions, and sustainably increase in data on food waste that occurs as a result of spoilage,
biomass. Some fungal species are known to persist under highlight the need for continued efforts in the area of food
the most extreme physiochemical conditions and thermal mycology. Decisions surrounding quality control programs
processing regimes used in commercial food production. are made throughout the manufacturing process, from
Yeast and filamentous fungi have proved particularly well determination of ingredient quality specifications prior to
suited to dispersion and cross-contamination within the food receipt and establishment of the processing conditions to
shipping and handling practices and sanitation programs.
processing infrastructure. Because of these diverse structural
Manufacturers often face fungal spoilage issues in raw
features and survival mechanisms, fungal species are well
ingredients and finished products (Table 1). The processing
adapted to particular ecological niches and are able to
history, packaging, formulation, and composition of the food
contaminate and spoil commercially processed foods.
all impact the likelihood of microbial spoilage and the
The burden of fungal food spoilage on the food industry relevant organisms. The intervention strategies used to
can be evaluated using several metrics. Fungal growth in control foodborne pathogens often contribute to the selection
processed foods, although typically not a food safety of food spoilage microorganisms. Many of the most resistant
concern, contributes to waste and loss throughout the supply spoilage microorganisms, capable of growing in seemingly
chain, is the cause of recalls and perishability, and can lead inhospitable environments, are fungi. This review summa-
to consumer dissatisfaction and mistrust of food manufac- rizes some of the predominant challenges concerning the
turers and retailers. Approximately 25% of the global food management of spoilage fungi within the food processing
supply is wasted or lost because of postharvest microbial environment. Specifically, issues relating to growth in
spoilage (18). This percentage differs among products based processed food and cross-contamination through air, water,
on formulation, processing, packaging, and storage, but in a materials, and equipment used in food production environ-
survey of juice manufacturers in the United States and ments are addressed.
Europe, 92% reported mold or yeast spoilage in the finished
product and 89% reported ingredient spoilage (33). There is FUNGI ARE PROBLEMATIC SPOILAGE
a significant need for quantitative assessments of product- ORGANISMS IN PROCESSED FOODS
specific food waste due to various factors. In contrast, food The impact of fungal spoilage in processed food is
safety issues are reported to regulatory agencies, and significant, given the inherent selection criteria imposed on
relatively extensive data exist on the incidence of foodborne the environment by formulation and processing. Fungi can
cause spoilage in products not believed to support growth (8,
* Author for correspondence. Tel: 330-263-3831; Fax: 330-263-3667; 17, 19, 37). Fungi proliferate in foods with extremely limited
E-mail: [email protected]. water availability and can cause spoilage in foods that are
1036 SNYDER AND WOROBO J. Food Prot., Vol. 81, No. 6

TABLE 1. Common names for commercial food spoilage issues and the associated causative fungus and quality deviation
Issue Description Scientific name Reference(s)

Machinery mold Accumulation of white or black mold on Geotrichum candidum 35

processing equipment; can cause off-
flavors and dextran production; has been
associated with dairy, fruits, and
vegetables and frozen food processing
environments
Chalk mold Surface spoilage of bread identifiable by Pichia burtonii and others 13, 30
white or pink patches
Thread mold Fungal growth in the small wrinkles of Mycelial growth of several common 21, 22
plastic packaging, often associated with molds: Phoma, aspergilli,
cheese penicillia
Puffballs Mold growth at the bottom of beverage Mycelial growth, often associated 33
containers; sometimes described as a with Paecilomyces
‘‘mouse in my product’’ or similar terms (Byssochlamys) growth in heat-
by consumers due to the dense treated juices
filamentous appearance
Mat Mold growth at the top of beverages or Pellicle: aerobic growth of one or Reported by
other fluids; associated with beer, pickles, more fungi industry
and other fermented vegetables
Black mold Powdery, black contamination resulting Aspergillus niger, Stachybotrys 1
from profuse conidiation
Blown pack spoilage Swollen container resulting from gas Yeast spoilage, very rarely 33
production (often but not always CO2) filamentous fungi
associated with fermentation and growth;
in extreme cases the package will rupture
under the increased pressure
Belly burst Anchovy belly explodes due to proteolysis Combination of fungi and bacteria 16
and gas production
Film yeast Thin pellicle growth on the high-oxygen Several oxidative yeasts form films: 3
interface between product and headspace Candida, Pichia
Food splash Spoilage of shelf-stable hot-filled products Typically aerobic, heat-sensitive 6
due to product splashing on the lip of the molds: Aspergillus, Penicillium,
container, compromising the seal integrity Cladosporium
and creating a conduit for spoilage fungi
Leaker spoilage Container bloating due to gas production Gas-producing spoilage fungi 6
of postprocessing contaminants introduced and bacterial spore formers
via seam defects, lack of pressure control,
and poor quality cooling water
Cat hair Defect on the surface of cheeses characterized Mucor and Rhizopus spp. Reported by
by the aerial hyphae of mucoralean fungi industry

very nearly pure water. Mineral water and aqueous solutions products, which are the ingredients in commercial food
of organic acids can support fungal growth, despite the production, rather than as hazards commonly associated
seeming lack of all but residual nitrogen (7). Fungi also can with finished product spoilage (5). However, increased
survive and infiltrate into commercially sterile foods because scrutiny of the safety risks associated with fungal growth in
of the extreme heat resistance of some fungal propagules and finished processed foods has led to more restrictive food
the profuse aerosolization of others. safety guidance and an increased demand for microbial risk
Although food spoilage is the primary concern with assessments (38).
fungi, several issues related to safety exist but are not often Various processing and formulation strategies have
discussed. Fungi are not considered biological hazards, but been used to reduce the diversity of microorganisms capable
several otherwise commensal fungi are opportunistic of proliferation under food production conditions. Food
pathogens (4). Acidified products (39) contain organic acids production strategies are frequently designed to control
that may support the growth of fungi (26). The breakdown bacterial pathogens, but many spoilage organisms are more
of these acids by fungal metabolism increases the pH of the resilient. Perhaps the earliest example of a commercial
product and can facilitate the growth of pathogenic bacteria processing technique designed to control spoilage microor-
(6). Mycotoxins are considered chemical hazards but are ganisms is the water bath canning method pioneered by
characterized primarily by their formation in raw agricultural Nicolas Appert in the late 1700s for use by the French
J. Food Prot., Vol. 81, No. 6 FUNGAL SPOILAGE IN FOOD PROCESSING 1037

military to preserve food for long expeditions (6). The prevent drafts, under tables for leveling, or under employee
challenges posed by fungal food spoilage today are workstations to provide cushion, all uses represent an
augmented by the demands of emerging food production unnecessary introduction of potential contaminants and are
and distribution systems, although our ability to identify and usually associated with the additional failure of another
control specific spoilage organisms has improved since prerequisite program within the facility.
Appert’s time due to the advent of molecular techniques and Some fungi are particularly associated with buildup on
international taxonomic consensus (15). processing equipment made of stainless steel, plastic, or
rubber. Geotrichum candidum collects on fan blades, air
OPPORTUNISM IN THE FOOD PRODUCTION vents, and rubber seals in food processing environments and
AND PROCESSING ENVIRONMENT is commonly known as machinery mold (Table 1).
Resembling dust or dirt accumulation, G. candidum can
As a consequence of the structural and metabolic
cause flavor changes if permitted to grow in food products.
features of fungi, these organisms are well adapted to
Cleaning procedures targeting G. candidum, as with all
proliferate within food production environments and within
sanitation programs, should take into consideration the
the products themselves. Elements of the food processing
potential for cross-contamination. After cleaning surfaces
infrastructure, from equipment and packaging materials to
contaminated with G. candidum (e.g., fan blades and air
processing water and air circulation systems, have been
vents) that are adjacent to processing equipment, facilities
associated with spoilage incidents in a variety of products
may notice a temporary increase in airborne mold spores due
(32). Many of these quality failures have resulted from poor
to aerosolization and may consequently reevaluate the
sanitation practices and were resolved through reevaluation
timing of product exposure.
of sanitation and good manufacturing prerequisite programs.
Some species of filamentous fungi and yeasts are
Monitoring records for visual inspections of cleanliness and
associated with the internal surfaces of processing equip-
tracking trends in total yeast and mold counts or other
ment contacted by the product and are difficult to clean.
indicators in the environment or finished product are useful
These surfaces include ports, valves, filler heads, and
for assessing the efficacy of these prerequisite programs. gaskets, which require disassembly to properly clean and
Aspects of manufacturing that may be important areas of serve as barriers or interfaces between the product and the
focus for fungal contamination control are discussed below. environment. Regions where proper circulation during
processing and cleaning in place are essential for sanitation,
MATERIALS AND EQUIPMENT
including potential dead legs and tubular heat exchangers,
Fungi are harbored by materials and equipment are areas where biofilms can lead to product contamination
commonly used in food production. Porous organic (25). Yeasts can contaminate the filler due to adhesion, and
materials, known to be problematic, are still used exten- the potential for yeast biofilm formation and persistence in
sively in secondary shipping containers, i.e., wooden pallets processing equipment is addressed through rigorous sanita-
or crates for storage and paperboard fillers and slip sheets. tion that is appropriate for the product, potential spoilage
For those items that are reused, cleaning and sanitation has organisms, and equipment design (40). As a functional
limited efficacy. The apple industry has traditionally relied category, black yeasts are commonly associated with water
on wooden bins during long periods of cold storage. handling systems and form recalcitrant biofilms in dead legs
Secondary apple pathogens that colonize the fruit after and over filters, grates, and nozzle heads (11, 20). Use of
harvest and senescence, notably Penicillium expansum and heated clean-in-place systems allows for treatment of
Byssochlamys spp., are transferred between seasons as the adjacent surfaces, whereas specific cleaning solutions may
fungal population builds on the wooden surface, effectively be more or less useful on processing equipment that handles
inoculating subsequent lots (25). These fungi are known high concentrations of lipids, proteins, calcium, or high-acid
mycotoxin producers, and wooden bins and crates can foods. Consultation with the equipment manufacturers and
contribute to violative concentrations of patulin in the final sanitizer providers will help ensure selection of an
product. However, many orchards have already made capital appropriate strategy.
investments in these systems, and total elimination of
wooden equipment may not be realistic or feasible. AIR AND WATER
Cardboard and paper materials used in packaging or Air and water throughout the facility serve effectively as
shipping also are notorious harborage sites for fungal spores. vectors for dispersion of fungi. Air handling systems may be
The highest level of heat-resistant molds in a production in place to maintain positive pressure over production, or air
facility is around the depalletizer (12, 28). Facilities with the may be filtered through a high-efficiency particulate air
space and resources will often physically separate this area system. Airborne molds can be particularly challenging
from the rest of the food processing environment to prevent during filling, and many facilities choose to cover and
inoculation of exposed product with fungal contaminants. contain their fill step, segregating it from the rest of
Temporary or retrofitted equipment is often of poor design production. Lack of air pressure controls has been associated
and integrates construction materials that are hard to clean with fungal spoilage (40). Compressed air used to remove
and may harbor spoilage fungi. Although this equipment debris from packaging or stationary food contact surfaces
may be utilized infrequently or only temporarily throughout should be considered for its contribution to microbial
the facility such as using tape to temporarily affix or hold quality. Blast freezers, which move air at high velocities,
items in place and placing cardboard slipsheets near doors to have also been a source of product contamination (9).
1038 SNYDER AND WOROBO J. Food Prot., Vol. 81, No. 6

Prolific conidia producers can be ubiquitous in the referred to as leaker spoilage (Table 1). Pinholes or
environment. Aspergillus, Cladosporium, and Penicillium microcracks may form momentarily along seams during
spores can be found in every cubic meter of air (41). The retort, introducing microscopic amounts of extraneous water
density of spores in an area varies seasonally and is highest (6). For this reason, many processors have elected to use
during spring and summer (2). Mold spores constitute 95% breakpoint chlorination in their processing water to
of the aerial microbiota over fruit orchards. The spread of inactivate potential contaminants. The organic load in
aerosolized mold spores can be managed through various processing water is greatly influenced by recirculation and
design and sanitation programs (24). Segregation of the frequency with which containers rupture, releasing
depalletization and shipment from the production floor and product into the system.
segregated and covered areas where product is filled into the
final container can help reduce the potential for airborne SANITATION PROGRAMS
fungal contamination. Segregation of dry or powdered Lax sanitation regimes are responsible for most of the
ingredients during storage and when measuring ingredients spoilage issues associated with commercially processed food
during batching can likewise help reduce the amount of air (34). Without effective sanitation, fungal populations will
particulates (9). Dry sanitation regimes have limited efficacy build up within the production system and become
against fungi (28); however, sanitation regimes such as dominated by spoilage fungi that proliferate well on the
fogging may prove particularly useful for reducing the food substrate. The dormant spore state also facilitates
airborne mold spore load. Air quality systems should be fungal persistence in processing environments because die-
monitored for efficacy. Consultation with the equipment off from environmental exposure is limited. Without rapid
manufacturer will help ensure employment of appropriate
and consistent elimination of harborage sites, persistent
monitoring techniques. Monitoring and verification activities
fungal spores collect within the environment until conditions
may include direct plating of pressurized air, determination
that support growth facilitate their germination. To eliminate
of filter change frequency, or quantitative air sampling.
organic debris and fungal niches, sanitizers should be
Water is another medium that can transfer fungal
selected based on the food composition and innate resistance
propagules within a facility, and water is associated more
of pertinent spoilage organisms. For example, the yeast-like
often than air with yeast cross-contamination. Yeasts are less
Zygosaccharomyces bailii is resistant to many common
likely to be introduced by air alone but may be carried in
sanitizers and preservatives, so for processors concerned
aerosols. Contamination due to splash and overspray during
about yeast spoilage (e.g., juice manufacturers), appropriate
sanitation programs is a major mechanism for the spread of
chemicals that have demonstrated efficacy against the target
spoilage yeasts. High levels of yeasts can frequently be
microbe should be used (26).
cultured from floor drains, and high-pressure sprays used for
Employee practices are predictors of food quality and
cleaning can splash contaminants onto processing equip-
have been associated with the presence of heat-resistant
ment (A.B.S. and R.W.W., unpublished data). For this
molds in raw agricultural commodities (22). Good manu-
reason, a final sanitizer rinse should be applied to processing
facturing practices for employee health and hygiene can
equipment after the floors have been cleaned. However,
influence the microbial quality of the product. Yeast
appropriate spray pressure can also reduce the movement of
spoilage from Candida and Hanseniaspora in fruit juices
spoilage organisms.
increased dramatically in samples taken from the processing
Insects also serve as a significant vector of yeast
environment compared with environmental and fruit sam-
contamination and should be controlled in production
ples taken from the orchard, putatively because of the
facilities (36). Insects are attracted to standing pools of
increase in yeast prevalence from the employees during
water or spilled product, which may be attractants when not
harvest and processing and more generally from yeast
rapidly removed or and when poor quality or poorly handled
raw products are used. Moisture should generally be limited contamination within the built environment (40). Further
within production facilities through air conditioning and testing revealed that although only 7.4% of the yeast strains
temperature control. Condensation formed over production isolated from the orchard were osmotolerant, 71% of the
lines or in cooling units serves as a conduit for yeast cross- yeast strains from the processing environment were
contamination. Proper cooling of finished products also can osmotolerant. Product-associated nutrients act as a selective
help reduce formation of condensation and the ingress of pressure, limiting the diversity of pertinent spoilage fungi
spoilage organism into products. Yeast spoilage has been within the facility and increasing the population of well-
found in products where moisture has introduced contam- adapted spoilage microbes (27, 31, 40).
inants from packaging and closures (23). Active cooling
FUNGUS PROSPECTUS
systems that use circulating water, such as cooling tunnels,
cooling towers, or cooling sprays, can introduce spoilage Continuing work in spoilage mycology will aid in the
organisms into finished product through this same mecha- development of targeted food quality programs that reduce
nism. The microbial quality of the water supply should be contamination and the growth of yeasts and filamentous
managed because the water is intentionally applied to the fungi. This work faces several technical barriers to analysis
container surface. Although that water is not intended to of root causes of contamination following a spoilage
reach food contact surfaces, the cooling food inside the incident and to targeted process development for the
container may draw in water as the vacuum forms, prevention of spoilage incidents. Morphological identifica-
particularly when the incipient seal is disturbed, commonly tion of fungi is exacting and time-consuming and often not
J. Food Prot., Vol. 81, No. 6 FUNGAL SPOILAGE IN FOOD PROCESSING 1039

practical in industrial applications. Morphological typing terephthalate for shelf-stable beverage packaging, which
should include examination on multiple media with lacks a true hermetic seal, permits the ingress of atmospheric
comparison of growth rates and characterization of conidia oxygen (23); decreases in can and plastic thickness increase
formation, ascospore shape, and the presence or absence of the probability of container damage and may decrease the
chlamydospores through microscopic examination (29). maximum fill temperature that the packaging is able to
Although these evaluations may provide useful information, withstand, which likewise impacts the formation of a
they also require an extensive knowledge of mycology. hermetic seal (14). Recycled and reuse packaging programs
Molecular methods may be faster, although growth of a may meet a growing interest in waste reduction. However,
pure culture is still needed. However, sequencing of internal these reused containers may be a significant source of
transcribed spacer regions, the consensus barcode regions spoilage fungi particularly suited for growth within the
for fungi, often produces resolution to only the genus, which product. Cleaning and sanitation programs for these
can minimize the utility of the findings. Amplification of containers should be rigorous and performed in a location
additional regions can be used to identify the species, but separate from the production area (23). However, environ-
this additional typing may again necessitate case-specific mental concerns over the use of abrasive cleaning solvents
consideration to select appropriate secondary amplicons and can represent competing interests. Likewise, rigorous cull
require PCR optimization due to variability among strains. programs to standardize ingredient quality may reduce the
Reliable and universal subtyping methods, such as random probability of fungal spoilage but has trade-offs regarding
amplification of polymorphic DNA or allelic typing, to trace food waste and ingredient specification costs (33). Solutions
spoilage organisms back to point sources are lacking in both to these and future challenges will need to include
the food and medical mycology fields. Misleading pheno- consideration of the mechanisms by which fungi persist in
typic information, such as the somewhat erroneous assump- highly restrictive food-relevant environments and should be
tions that oxygen-limiting conditions completely control the congruous with changing ecological and social attitudes. A
growth of filamentous fungi and that a spoilage mold dedicated increase in resource allocation to address fungal
isolated from a hot filled product is necessarily heat resistant, spoilage of food is needed. Food mycology is a small subset
further complicate the ability of processors to perform root of the larger food microbiology field, and the educational
cause analysis. Rapid and sensitive identification methods pipeline for producing researchers with either classical
would facilitate the tracking of background mycobiota as training or hands-on expertise has not kept pace with the
part of a preventative quality control program. challenges posed by fungi in contemporary food production.
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