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Preventing stored-product insect infestations in packaged-food products

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 Stewart Postharvest Review
An international journal for reviews in postharvest biology and technology

Preventing stored-product insect infestations in packaged-food products

Christos G Athanassiou1*, Jordi Riudavets2 and Nickolas G Kavallieratos3

1
Laboratory of Entomology and Agricultural Zoology, Department of Agriculture, Crop Production and Rural Environment,
University of Thessaly, Phytokou str., Nea Ionia, Magnissia, Greece
2
IRTA, Entomology, Ctra. Cabrils Km 2, Barcelona, Spain
3
Laboratory of Agricultural Entomology, Department of Entomology and Agricultural Zoology, Benaki Phytopathological Institute,
Kifissia, Attica, Greece

Abstract
Purpose of review: The present review provides an overview of insect pest species associated with packaged-food products, potential
mechanisms leading to infestation of packaged products, and strategies to prevent such infestation.
Findings: There are two possible reasons that may explain the presence of insects in packaged products: (1) insects are present in the
product before packaging, or (2) insects invaded the product after packaging from already existing openings or from insects creating an
entry point. Control strategies include the correct identification of the species found in the packaged product, mechanical or thermal
methods for eliminating infestations in raw and processed products, use of repellents or insecticides outside packages, and application
of modified or controlled atmospheres inside packages.
Directions for future research: Further research is required on the above topics focusing on all stages of food manufacture and distri-
bution for successful prevention of insect presence in packaged products.

Keywords: food packaging; penetrators; invaders; insect-proof packaging; food safety; pest prevention; pest cross-contamination

Abbreviations Introduction
MAP Modified Atmosphere Packaging The presence of stored-product insect pests in raw and pro-
PVC Polyvinyl Chloride cessed commodities can cause serious qualitative and quan-
titative losses. Several insect species are able to infest amy-
*Correspondence to: Christos G Athanassiou, Laboratory of laceous commodities and commodities of high sugar con-
Entomology and Agricultural Zoology, Department of Agri- tent, such as dried fruit [1]. Apart from the infestation per
culture, Crop Production and Rural Environment, University se, insects cause additional damage, such as altering temper-
of Thessaly, Phytokou str., Nea Ionia, 38446, Magnissia, ature, moisture/humidity level and microflora of the infested
Greece. Tel. +30-2421093195; Fax: +30-2421093195; commodity through their metabolism and multiplication.
email: athanassiou@[Link] Insects in raw commodities are easy to manage, but every
effort should be made to prevent insects or insect parts in
Stewart Postharvest Review 2011, 3:8 finished products. For example, the presence of live insects
Published online 01 December 2011 or insect contamination (body parts, faecal material, etc) in
doi: 10.2212/spr.2011.3.8 finished products, besides being unacceptable to unsuspect-
ing consumers, are governed by federal food regulations,
and in extreme cases, may make food unsuitable for con-
sumption [2]. Stored-product insect pests are also vectors of
several diseases that may endanger human or animal health.
For example, Larson et al. [3] indicated a noticeable pres-
ence of enterococci, which are reservoirs for potentially
© 2011 Stewart Postharvest Solutions (UK) Ltd.
Online ISSN:1945-9656
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Athanassiou et al. / Stewart Postharvest Review 2011, 3:8

virulent and antibiotic resistant genes, in stored-product in- toothed grain beetle, Oryzaephilus surinamensis (L.); red
sects. In developed countries the presence of insects in pack- flour beetle, Tribolium castaneum (Herbst); and the cowpea
aged food products can discredit the image of the product or weevil, Callosobruchus maculatus (F.), were able to penetrate
the manufacturer of the product, make the food non-compliant polyethylene that was less than 0.08 mm in thickness. Gener-
with established food regulations, and may have adverse eco- ally, among multilayer, polyester, polyethylene and polypro-
nomic impacts to the manufacturer in terms of product re- pylene the available data clearly indicate that multilayer and
placement and lawsuits. There are numerous examples of in- polyethylene were by far the least and most susceptible to
sects in processed dry, durable packaged commodities. There penetration, respectively, by stored-product beetle species [7].
may be several reasons for such infestation and a thorough However, larvae of stored-product moths, such as the almond
investigation of the entire supply chain may provide possible moth, Cadra cautella (Walker); and Indian meal moth, Plodia
clues as to the source of infestation. Some issues could be interpunctella (Hübner), were unable to penetrate polypropyl-
related to sanitation, improper care during packaging, or cross ene films [9]. These results indicate that adults of R. dominica
-infestation in retail stores [4]. However, the mechanisms that and L. serricorne can penetrate several types of plastic films,
determine the presence of stored-product insects in packaged and to some extent, multilayer films with greater ease than the
food may differ, according to the type of commodity, the in- other species. Therefore, these species can be classified as
sect species and the type of the packaging material. “true penetrators” [6, 7]. In contrast, most of the common
stored-product insects usually enter packaged food through
Package penetrators and invaders already existing holes or openings/imperfections at seals.
Various plastic films have been tested for their ability to pro- Therefore, such species can be considered as “invaders”. For
tect products from insect infestation. The most important plas- example, O. surinamensis adults usually do not chew the plas-
tic materials in use for food packaging are polyethylene, poly- tic in order to create holes, but enter from already existing
propylene and polyester [5]. However, paper and multilayer holes [11]. Adler [12] noted that, with the exception of young
packages, containing additional materials, such as aluminium larvae, most of the species that usually occur in packaged
foil, are also used extensively for various value-added prod- products cannot pass through holes that are less than 0.71 mm
ucts. Riudavets et al. [6] tested the ability of the rice weevil, in width. Generally, neonate larvae (first instars) are able to
Sitophilus oryzae (L.); lesser grain borer, Rhyzopertha domi- invade polyethylene, polypropylene and polyvinyl chloride
nica (F.); and cigarette beetle, Lasioderma serricorne (F.), in (PVC) through holes of minimal size, which are often less
penetrating different packaging materials (Figure 1). Based on than 0.5 mm in diameter [12]. This is particularly important in
this work, all species, at the adult stage were considered as the case of the packages that are deliberately punctured to
penetrators of polyethylene (50-µm thick), polypropylene (25- allow gas exchange during fumigation or controlled or modi-
µm thick) and polyester (12-µm thick). Generally, R. domini- fied atmosphere treatment of rooms in which the packages are
ca and L. serricorne adults were able to penetrate plastic films stored. In fact, all packaged products have openings to accom-
better than adults of S. oryzae. Moreover, the larvae of L. ser- modate pressure differences that occur at different elevations
ricorne were not able to create holes in polyester. At the same or during transportation in airplanes. Another reason for hav-
time, the increase in thickness of the material decreased the ing openings in packages is to facilitate proper stacking on
penetration ability by the above species [7]. On the other pallets or retail store shelves. Some packages are stitched or
hand, Shukla et al. [8] noted that adults of S. oryzae, R. domi- glued by heat seals. Packages with stitches provide easy ac-
nica, the Khapra beetle, Trogoderma granarium Everts; saw- cessibility to stored-product insects. If the glue seals are dis-
continuous, insects can use areas where there is no glue as
pathways for infestation. Despite packaging issues, it is also
important to eliminate infestations in transportation vehicles
and retail stores to prevent cross-infestation from these
sources into packaged products. Several issues of infestation
Figure 1. Holes in polypropylene film made by Sitophilus oryzae.
in packaged products have been traced back to infestations in
transportation vehicles and retail stores.

Critical stages for package infestation

The presence of insects in packaged products does not neces-
sarily mean that insects penetrated or entered the package
through already existing holes. The shape of the hole and
fraying of the hole are often indicative of the direction of
insect movement, ie, if the insects are entering or exiting
from a package. Riudavets et al. [6, 7] overviewed the char-
acteristics of the entrance or exit holes that are produced by
some major stored-product beetle species. Hence, there are
two broad scenarios that may explain the presence of insects
in packaged products [13].
2
Athanassiou et al. / Stewart Postharvest Review 2011, 3:8

In the first scenario, insects were present in the product before be related with toxins, quinones and other excretions [20].
it was packaged, suggesting infestation of raw commodities or Apart from insects, the presence of insect by-products and
cross-infestation during processing. Furthermore, infestation mites or their by-products can lead to allergic reactions [21].
could occur from insects that are present in the packaging
materials. An example is corrugated cardboard paper used for Management of insects in packaged products
boxes [12, 13]. The corrugations provide an ideal site for in- The identification of the species found in packaged products
sects to hide or pupate. Insect infestation in raw commodities should be the first step in developing methods for preventing
is common, and care must be exercised when receiving raw package infestations [6]. A thorough understanding of where
commodities through visual inspection of the raw material at and when the infestation occurred will help in determining
the food-processing facility [14]. This scenario is more likely critical control points for intervention to reduce or eliminate
to occur in the commodities where the processed material to insect pest infestation. The reduction of the size of the hole,
be packaged does not undergo any thermal treatment during or even the elimination, if possible, of the holes in the pack-
processing. For example, packaging of already infested prod- age, can act as a “barrier” in many cases [11, 12]. The elimi-
uct is common with milled rice. In rice, although during the nation of holes in pasta packages may help to drastically re-
conventional polishing process high mortality is generated in duce the infestation levels by S. oryzae. Insect-resistant pack-
the weevil population (>95%), some insect eggs may survive aging with suitable materials may prevent infestation; cur-
in the final product [15]. Athanassiou [16] indicated that the rently there are several materials that are commercially avail-
majority (>80%) of the insects that existed in packaged rice able for this purpose [17, 22]. Hou et al. [23] successfully
belonged to S. oryzae and O. surinamensis, which are species tested insect repellents that were applied to packages, while
that are not usually able to chew holes in plastic films. Moreo- application of low-risk insecticides may also be effective
ver, it is well known that several moth species utilise packag- [24]. The use of an odour barrier as an over-wrap, especially
ing materials as refugia (places to hide) or overwintering loca- for boxed-products, has helped in drastically reducing infes-
tions [12]. Therefore, moth infestations can be due to larval tations of P. interpunctella larvae (Bhadriraju Subramanyam,
presence in packaging materials (plastic or paper). Mullen and unpublished data).
Mowery [17] noted that female P. interpunctella can locate
packages that contain food in comparison with packages that The use of modified and controlled atmosphere is one of the
contain non-food items, because of odours emanating from solutions suggested. In a laboratory study, New and Rees
the packaged product. [25] have already shown the ability of three different types of
modified atmosphere packaging (MAP) to control C. macula-
In the second scenario, insects can invade the product after tus in cowpeas, T. castaneum in wheat flour, and R. dominica
packaging at locations far removed from where the product in wheat. Jayas and Jeyamkondan [26] noted that T. castane-
was manufactured. This scenario is more complex and re- um, the confused flour beetle, Tribulium\confusum (Jacquelin
quires the existence of holes or the use of inappropriate plas- du Val) and O. surinamensis could be controlled at >99% N2
tic materials that are too thin. In this scenario, there are plau- and <1% O2. At the same time, >90% CO2 and <10% O2
sible reasons for insect presence inside packages. Insects may could control C. ferrugineus and S. oryzae, but the mortality
have entered the package from already existing holes or gaps increased with decreasing moisture [22, 26]. Nevertheless,
in packaging, or insects created an opening by chewing the moisture/humidity changes may affect quality characteristics
packaging material. These situations can occur in distribution in less durable products, such as dried fruit. Oxygen scaven-
centres, warehouses, and retail stores where the packaged gers can be used with success as a means of achieving modi-
products are held or sold. fied atmosphere conditions within the package, especially in
the case of dried fruits, a procedure which is known as
In a screening in packaged pasta products from several coun- “active packaging” [27]. Locatelli and Daolio [28] found that
tries of southern Europe (Athanassiou, unpublished data), S. CO2 with reduced pressure was able to control R. dominica,
oryzae was the main insect found (>90% of the cases exam- S. oryzae, O. surinamensis and P. interpunctella while eggs
ined). In those facilities, even if the raw grain was infested of R. dominica and old larvae and pupae of P. interpunctella
with S. oryzae, processing to semolina or pasta involves sev- were the least susceptible life stages. Generally, in the case of
eral treatments that often kill all insect stages (eg, tempera- amylaceous commodities, the application of modified or con-
tures >50oC for several hours) [18]. Hence, the final product trolled atmospheres in packages has negligible adverse ef-
is usually pest-free, and any infestation may be due to how fects on the quality of amylaceous commodities than on dried
the product was handled after the thermal treatment at the fruit [22, 29]. Riudavets et al. [30] found that 50% CO2 in
facility or how it was handled during transport and in distri- plastic packages was effective against L. serricorne, C. ferru-
bution centres, warehouses, and retail stores. gineus, O. surinamensis, T. confusum, R. dominica, S. oryzae,
the Mediterranean flour moth, Ephestia kuehniella Zeller; P.
Apart from the presence of live insects, other insect-related interpunctella, the psocid Liposcelis bostrychophila Badon-
contaminants can also occur in packaged products. For in- nel and the cheese mite, Tyrophagus putrescentiae (Schrank).
stance, insect fragments can be present, especially from the Of the life stages tested, L. serricorne pupae and eggs and T.
raw products [19]. Other contaminants involving insects may putrescentiae eggs were less susceptible than the life stages
3
Athanassiou et al. / Stewart Postharvest Review 2011, 3:8

of the other species. Moths were controlled more easily than interpunctella (Lepidoptera: Pyralidae) larvae, and Tribolium confusum
(Coleoptera: Tenebrionidae) adults. Journal of Economic Entomology
beetles, psocids and mites. Riudavets et al. [31] reported that
1997: 90: 1028–1031.
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10 Cline LD and Highland HA. Minimum size of holes allowing passage of
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Society 1981: 16: 521–524.
Conclusions 11 Adler C. Significance of hermetic seals, controlled ventilation, and wire-
Several stored-product insect pests are capable of invading or mesh screens to prevent the immigration of stored product pests. IOBC/
WPRS Bulletin 2004: 27: 13–16.
penetrating packages to infest the product contained within.
12 Adler C. Insect-proof packaging to avoid stored product insects. IOBC/
The presence of insects can be explained by two simple rea-
WPRS Bulletin 2008: 40: 363–369.
sons: (1) insects were already present in the product before it
13 Mueller DK. Reducing Customer Complaints in Stored Products. West-
was packaged at the facility where it was processed or (2) field, Indiana: Insects Limited Inc. 2010.
insects invaded or penetrated the package after the packaged 14 Mueller DK. Stored product protection: a period of transition. Indianapo-
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curred. Therefore, it is important for manufacturers to keep process on Sitophilus oryzae (Coleoptera: Curculionidae). Journal of
track of complaints relating to infestations in packaged prod- Economic Entomology. 2000: 93: 1837–1841.
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