ArticlePDF Available

Carbon Dioxide Fumigation for Controlling Bed Bugs

Authors:

Abstract and Figures

We investigated the potential of carbon dioxide (CO2) fumigation as a method for controlling bed bugs, Cimex lectularius L. The effect of bed bug developmental stage, temperature, and CO2 concentration on the minimum time to kill 100% of bed bugs was determined. The minimum CO2 concentration lethal to all bed bug stages was approximately 30% with 24 h exposure time at 25 degrees C. The minimum fumigation time required to kill 100% of eggs using 100% CO2 at 20, 25, and 30 degrees C were 3, 7, and 8 h, respectively; the minimum fumigation time to kill 100% of adult males/nymphs were 8, 13, and 14 h, respectively. The minimum time to kill 100% of adult males/nymphs using 50 and 70% CO2 at 25 degrees C were 18 and 16 h, respectively. We found that eggs were not completely killed after 24 h fumigation when the CO2 concentration was lower than 80%. Thus, bed bug eggs were more susceptible to 100% CO2 fumigation than nymphs and adult males but more tolerant than nymphs and adult males with lower CO2 concentration (50-80%). There were no significant differences among nymphs, adult males, and adult females in their susceptibility to 100% CO2 fumigation. A 24 h fumigation in sealed 158 liter (42 gallon) heavy duty garbage bags filled 90% full with fabric materials and/or boxes and 1,350 g dry ice per bag was sufficient to kill all stages of bed bugs hidden in the materials at room temperature (23-24 degrees C). Sealed heavy duty garbage bags maintained > or = 94% CO2 for at least 24 h. Custom-made double zipper plastic bags (122 x 183 cm) were also used to evaluate the effectiveness of CO2 fumigation for controlling bed bugs. Each bag was filled with fabric and boxes to 50-90% full. Bed bugs were hidden in various locations of each bag. CO2 was introduced into the bags through a CO2 cylinder. CO2 fumigation lasting 24-48 h was sufficient to kill all stages of bed bugs at room temperature, depending on the quantity of materials placed in each bag and whether CO2 was introduced one or two times at the onset. CO2 is an effective alternative to conventional fumigants for eliminating bed bugs hiding in infested household items such as clothing, shoes, books, electronics, sofas, and so forth.
Content may be subject to copyright.
VECTOR CONTROL,PEST MANAGEMENT,RESISTANCE,REPELLENTS
Carbon Dioxide Fumigation for Controlling Bed Bugs
CHANGLU WANG,
1
LIHUA LU
¨,
2
AND MING XU
3
J. Med. Entomol. 49(5): 1076Ð1083 (2012); DOI: http://dx.doi.org/10.1603/ME12037
ABSTRACT We investigated the potential of carbon dioxide (CO
2
) fumigation as a method for
controlling bed bugs, Cimex lectularius L. The effect of bed bug developmental stage, temperature,
and CO
2
concentration on the minimum time to kill 100% of bed bugs was determined. The minimum
CO
2
concentration lethal to all bed bug stages was 30% with 24 h exposure time at 25C. The
minimum fumigation time required to kill 100% of eggs using 100% CO
2
at 20, 25, and 30C were 3,
7, and 8 h, respectively; the minimum fumigation time to kill 100% of adult males/nymphs were 8, 13,
and 14 h, respectively. The minimum time to kill 100% of adult males/nymphs using 50 and 70% CO
2
at 25C were 18 and 16 h, respectively. We found that eggs were not completely killed after 24 h
fumigation when the CO
2
concentration was lower than 80%. Thus, bed bug eggs were more
susceptible to 100% CO
2
fumigation than nymphs and adult males but more tolerant than nymphs and
adult males with lower CO
2
concentration (50Ð80%). There were no signiÞcant differences among
nymphs, adult males, and adult females in their susceptibility to 100% CO
2
fumigation. A 24 h
fumigation in sealed 158 liter (42 gallon) heavy duty garbage bags Þlled 90% full with fabric materials
and/or boxes and 1,350 g dry ice per bag was sufÞcient to kill all stages of bed bugs hidden in the
materials at room temperature (23Ð24C). Sealed heavy duty garbage bags maintained 94% CO
2
for
at least 24 h. Custom-made double zipper plastic bags (122 183 cm) were also used to evaluate the
effectiveness of CO
2
fumigation for controlling bed bugs. Each bag was Þlled with fabric and boxes
to 50Ð90% full. Bed bugs were hidden in various locations of each bag. CO
2
was introduced into the
bags through a CO
2
cylinder. CO
2
fumigation lasting 24Ð48 h was sufÞcient to kill all stages of bed
bugs at room temperature, depending on the quantity of materials placed in each bag and whether
CO
2
was introduced one or two times at the onset. CO
2
is an effective alternative to conventional
fumigants for eliminating bed bugs hiding in infested household items such as clothing, shoes, books,
electronics, sofas, and so forth.
KEY WORDS Cimex lectularius, fumigation, carbon dioxide, control
Bed bugs (Cimex lectularius L. and Cimex hemipterus
F.) are very difÞcult pests to manage, in part, because
of their widespread resistance to insecticides and
cryptic behavior (Romero et al. 2007, Zhu et al. 2011).
Bed bugs are not limited to sleeping and resting areas
such as beds and sofas, instead virtually anything in the
structure is susceptible to infestation. It is not uncom-
mon to Þnd bed bugs in personal items such as elec-
tronics, books, pictures, piles of papers, small appli-
ances, furniture, and so forth. Eliminating bed bugs
safely and effectively from these types of items is often
more challenging than eliminating bed bugs hiding in
cracks and holes in furniture or the structure itself.
Current tools and methods for treating bed bug-
infested household items include discarding the in-
fested items, hot washing, freezing, hot drying, apply-
ing hot steam, placing items in heating chambers,
whole structure heating, applying pesticides, or fumi-
gation of infested items with sulfuryl ßuoride or di-
chlorvos (Doggett 2011). Each of these methods or
tools has some limitations (Table 1). There is a lack of
safe and effective methods for eliminating bed bugs in
infested household items.
ModiÞed atmosphere (MA) with high concentra-
tions of carbon dioxide (CO
2
) has been used in con-
trolling stored product insects (Adler et al. 2000, Na-
varro 2006, Riudavets et al. 2009, Navarro et al. 2012).
Elevated CO
2
levels cause insect spiracles to remain
open, resulting in death from water loss (Nicolas and
Sillans 1989). High CO
2
concentration also has toxic
effects on the nervous system of insects. The use of
MA has advantages over other toxic chemicals in that
MA leaves no residue and is less likely to damage the
fumigated materials. However, the use of MA is lim-
ited because of the requirement for air tight contain-
ers, and days or weeks of fumigation time. Herrmann
et al. (1999) reported preliminary results on the effect
of CO
2
fumigation against bed bugs. They found 60%
CO
2
caused 100% mortality to all bed bug stages within
1
Corresponding author: Department of Entomology, Rutgers
University, New Brunswick, NJ 08901 (e-mail: cwang@aesop.
rutgers.edu).
2
Plant Protection Research Institute, Guangdong Academy of Ag-
ricultural Sciences, Guangzhou 510640, China.
3
Department of Ecology, Evolution, and Natural Resources, Rut-
gers University, New Brunswick, NJ 08901.
0022-2585/12/1076Ð1083$04.00/0 2012 Entomological Society of America
Downloaded from https://academic.oup.com/jme/article-abstract/49/5/1076/1044970/Carbon-Dioxide-Fumigation-for-Controlling-Bed-Bugs
by guest
on 15 September 2017
24 h, suggesting CO
2
fumigation may be a viable ap-
proach for eliminating bed bugs from infested house-
hold items. The objectives of the current study were
to: 1) determine the lethal exposure time and mini-
mum lethal CO
2
concentration to kill bed bug eggs,
nymphs, and adults; 2) determine the effect of tem-
perature on the effectiveness of fumigation; and 3)
determine the efÞcacy of containerized CO
2
fumiga-
tion for control of bed bugs.
Materials and Methods
Insects. A laboratory and two Þeld strains of C.
lectularius were maintained in plastic containers (47
mm diameter, 47 mm tall) with folded Þlter paper as
harborages. The two Þeld strains (Jersey and Indy)
were collected 1 wk and 2 yr before this study, re-
spectively. The laboratory and the Indy strains were
fed weekly with deÞbrinated rabbit blood using an
artiÞcial membrane feeding system (Hemotek Ltd.,
England, United Kingdom). The bed bugs were kept
at 23Ð26C, 24Ð48% relative humidity (RH), and a
photoperiod of 12:12 (L:D) h environment. Before the
experiment, bed bug eggs of 0Ð8 d old along with the
paper substrate were carefully cut out and were trans-
ferred into 3.7 cm diameter, 1.0 cm tall plastic petri
dishes. Bed bug nymphs and adult males that were fed
3Ð9 d previously were transferred into the same dishes
as the eggs or into separate dishes. Bed bug adult
females were placed in separate dishes when used in
experiments. The dish lids and bottoms had 1.25 cm
diameter openings covered with Þne nylon screens to
allow for air exchange. The closed dishes were
wrapped using ParaÞlm Sealing Sheets (Bemis Flexi-
ble packing, Neenah, WI) to hold the lids and the
bottoms together during the experiments. Preliminary
tests indicate there were no signiÞcant differences
among the laboratory strain and two Þeld strains in
their mortality response to CO
2
fumigation. There-
fore, we used the laboratory strain in most experi-
ments. The Indy strain was used in a few experiments
when not enough laboratory strain bed bugs were
available.
Fumigation Containers. Four types of fumigation
containers were used in this study to evaluate the
effect of high CO
2
concentrations on bed bug survival
(Fig. 1). Pyrex Erlenmeyer ßasks (2000 ml volume;
VWR International, LLC, Bridgeport, NJ) were used
for evaluating the effect of 100% CO
2
fumigation.
Ziploc double zipper bags (3.7 liter volume) (SC John-
son, Racine, WI) were used for evaluating 50Ð90%
CO
2
. Heavy duty garbage bags (158 liter volume, 3 mm
thickness; Husky, PolyAmerica, Grand Rapids, TX)
were used for evaluating the dry ice treatment. Buga-
nator fumigation bags (122 183 cm, 3.5 mm thick-
ness) with double zippers (Protect-A-Bed, Chicago,
IL) were used for evaluating the CO
2
gas treatment.
Each Buganator bag has two 3 cm diameter openings
for connecting to a hose or power source.
Experiment 1: Minimum Lethal CO
2
Concentra-
tion. Mixed air containing 19.38 and 29.86% CO
2
(Air-
gas East Inc, Piscataway, NJ) were obtained to eval-
uate the effect of elevated CO
2
concentration on bed
bug eggs, nymphs, and adult males. Ten bed bug third
to Þfth instar nymphs, 10 adult males and 11Ð31 eggs
were placed in each petri dish. Ziploc double zipper
bags were used as fumigation container (Fig. 1). The
bags were checked for leakage before being used.
Each dish was placed in a separate bag and afÞxed to
middle portion with tape. Each bag was Þlled with
mixed air of known CO
2
concentration or natural
atmosphere. Three bags were tested for each concen-
tration. The bags were suspended from racks in an
incubator (model I36VL, Percival ScientiÞc, Inc.
Perry, IA) at 25C. A running fan located at the ceiling
of the incubator kept the bags moving during the
fumigation period, which prevented CO
2
from possi-
ble settling inside the bags. After 24 h, the bags were
removed from the incubator and the dishes were taken
out from the bags. They were blown brießy with a
table fan to remove high CO
2
levels inside the dishes.
The dishes were placed in a laboratory at 23.4 0.1C
and a photoperiod of 12:12 (L:D) h cycle. Bed bug
mortality and egg hatch was observed daily for up to
10 d after fumigation.
Experiment 2: Minimum Lethal Exposure Time to
Kill Bed Bugs With 100% CO
2
.Thirty grams dry ice
pellets were placed in each 2,000 ml ßask. A rubber
stopper was loosely placed on top of each ßask. After
sublimation was complete, the ßasks were immedi-
ately sealed tightly using rubber stoppers. Because
CO
2
is the densest component in the natural atmo-
sphere, the sublimation process would create a 100%
CO
2
environment inside the ßasks.
Before the fumigation treatment, the ßasks were
placed in a 30C incubator to bring the temperature of
the ßasks containing 100% CO
2
to the same temper-
ature as the incubator. Bed bugs were prepared as in
the previous experiment. Bed bug eggs and mobile
stages were placed in different dishes. Each dish con-
tained 10 males and 10 nymphs, or 14Ð29 eggs. One
Table 1. Current bed bug control methods and their limitations
for treating bed bug infested household items
Bed bug control
methods and tools Limitations
Hot steam May damage items such as books,
electronics, and furniture
Hot washing and
laundering
Cannot be used for nonwashable and
sensitive items
Discarding infested
materials
Impractical in many instances
Freezers or portable
heaters
Large items cannot be treated
Whole house heat
treatment
Very expensive
Insecticide sprays Will leave residues on treated surface and
are often ineffective after dried; may
not penetrate into harborages
Chemical fumigation Very expensive and requires extensive
training
Dichlorvos resin strips Slow (requires weeks of time) and may
corrode iron and steel (Hayes and
Laws 1990, Lehnert et al. 2011); may
cause discomfort to those with
respiratory diseases
September 2012 WANG ET AL.: CO
2
FUMIGATION FOR CONTROLLING BED BUGS 1077
Downloaded from https://academic.oup.com/jme/article-abstract/49/5/1076/1044970/Carbon-Dioxide-Fumigation-for-Controlling-Bed-Bugs
by guest
on 15 September 2017
dish was placed into each ßask and the ßask was
immediately resealed using a rubber stopper. Prelim-
inary tests showed eggs were killed within 2Ð4 h and
mobile stages were killed after 7Ð9 h fumigation at
30C. Therefore, we used 2.25, 3, 4, 5, 6, 7, and 8 h
fumigation time for eggs and 7, 8, and 9 h fumigation
time for nymphs/males. The fumigation time in the
control was 8 h for eggs and 9 h for nymphs/males. For
each exposure time, three ßasks were used. After fu-
migation, the bed bug dishes were taken out of the
ßasks and placed in a laboratory incubator at 23.4
0.1C and a photoperiod of 12:12 (L:D) h cycle for
observation of mortality daily for 14 d.
Experiment 3: Effect of 100% CO
2
Fumigation on
Bed Bugs at Different Temperatures. Similar to Ex-
periment II, bed bug eggs, nymphs, and adults were
subjected to 100% CO
2
fumigation at 25 and 20C using
2,000 ml ßasks. In the 25C test, each dish contained
8Ð15 eggs, 10 nymphs and 10 males or 10 females. We
included females in this experiment to evaluate
whether there are any differences among nymphs,
males, and females. The fumigation time evaluated
was 5, 6, 7, 8, and 9 h for eggs and 6, 7, 8, 9, 10, 11, 12,
13, 14, and 15 h for nymphs, males and females. The
eggs and mobile stages in the control were removed
from ßasks containing natural atmosphere after nine
and 15 h, respectively. For each exposure time, three
ßasks were used. The egg hatches were observed daily
until 3 d after no more eggs hatched.
In the 20C test, each dish contained 10 nymphs and
5 males, or 10Ð31 eggs. The fumigation time was 7, 8,
9, 10, and 11 h for eggs and 12, 13, 14, and 15 h for
nymphs/males. The eggs and nymphs/males in the
control were removed from ßasks containing natural
atmosphere at 11 and 15 h, respectively. For each
exposure time, three ßasks were used. The egg hatches
were observed daily until 3 d after no more eggs
hatched.
Experiment 4: Effect of 50 –90% CO
2
Fumigation on
Bed Bugs. The relationship between CO
2
concentra-
tion (49.32 and 71.38%) and time required to kill 100%
of the bed bugs were examined at 25C. Nymphs/
males were treated with 49.32 and 72.38% CO
2
. The
fumigation times evaluated were 10, 12, 14, 16, and 18 h
for 49.32% CO
2
, and 10, 14, and 16 h for 71.38% CO
2.
Ten nymphs and 10 males were placed in each dish.
One dish was placed in each Ziploc bag as in Exper-
iment I. Eggs were only treated with 71.38% CO
2
. The
treatment time was 12, 14, and 16 h. Ten to 23 eggs
were placed in each dish. Each exposure time was
replicated three times.
Because the above test resulted in very low egg
mortality, we further tested the effect of CO
2
fumi-
gation on eggs using higher CO
2
(78.96 and 89.64%)
concentration, higher temperature (30C), and longer
exposure time (24 h). Each dish contained 12Ð34 eggs.
Each CO
2
treatment was replicated three times.
Experiment 5: Efficacy of CO
2
Fumigation Against
Bed Bugs in Garbage Bags. This test was intended to
determine whether dry ice can be used as CO
2
source
for controlling bed bugs buried in household items.
Heavy duty 158 liter (42 gallon) sized garbage bags
were Þlled with pillows, clothing, and fabric sheets
(including one water proof fabric mattress cover) to
Fig. 1. Fumigation containers used in the study. (A) A 2,000 ml glass ßask with a petri dish containing bed bugs; (B) A
3.7 liter Ziploc bag with a petri dish containing bed bugs; (C) A 158 liter (42 gallon) heavy duty garbage bag Þlled with fabric
materials and three CO
2
sensors; (D) A Buganator fumigation bag 50% full of fabric materials and boxes, a laptop computer,
and three CO
2
sensors for recording CO
2
concentrations. (Online Þgure in color.)
1078 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 49, no. 5
Downloaded from https://academic.oup.com/jme/article-abstract/49/5/1076/1044970/Carbon-Dioxide-Fumigation-for-Controlling-Bed-Bugs
by guest
on 15 September 2017
90% full (22 kg materials) (Fig. 1c). Three petri
dishes containing bed bugs were placed in each bag at
three locations: top, center, and bottom. In the 900 g
dry ice treatment, each dish contained 10 Ð22 (average
15.6) eggs, 10 nymphs, and 10 males. Each dish was
placed into a cotton sock to minimize air exchange
inside the dishes. Nine hundred grams dry ice pellets
total were spread near bottom, at center, and at the top
of the fabric pile in each bag. Dry ice was not placed
in the control bags. Each bag was sealed by tightly
tying cotton string around the top of the bag to min-
imize air exchange between the air in the bags and the
air outside the bags during experiments. The bags
were placed in a laboratory with the sealed opening
directed upward. After 24 h, the bed bug dishes were
taken out of the bags and ventilated brießy using a
table fan, and then placed in a laboratory for obser-
vation of egg hatch or mortality of nymphs/males daily
for up to 10 d. The mean room temperature during the
24 h fumigation period was 23.6 0.1C. The treat-
ment and the control were replicated three times.
The above test did not result in 100% mortality of
the bed bugs. We further tested CO
2
fumigation using
1,350 g dry ice per bag. Each dish contained 10Ð15
eggs, 5 nymphs, and 5 males. Three dishes were placed
in each bag. The treatment was replicated six times
and the control was replicated four times. The room
temperature during the fumigation period was 23.0Ð
23.9C. Other procedures were the same as in the 900 g
dry ice treatment.
Three 0Ð100% CO
2
sensors (CO
2
Meter, Ormond
Beach, FL) were placed in three separate bags, each
with 1,350 g dry ice, to record CO
2
concentrations
every 10 min for 2 d (Fig. 1c). The Þrst two bags
contained 22 kg (per bag) fabric materials (pillows,
clothing, and sheets). The third bag contained a mix-
ture of fabric materials and two cardboard boxes that
were Þlled with empty round plastic (5.5 cm diameter,
4 cm tall) containers. All bags were 90% full. One
sensor was placed near the bottom of the fabric pile,
one was placed at the center, and one at the top. The
sensor at the center location was wrapped in water
proof fabric to simulate the most challenging situa-
tions where CO
2
penetration may be slow.
Experiment 6: Efficacy of CO
2
Fumigation Against
Bed Bugs in Custom-Made Fumigation Bags. Bugana-
tor (122 183 cm) bags were used to evaluate the
efÞcacy of CO
2
fumigation for eliminating bed bugs
buried in household items. These bags have resealable
double zippers and can accommodate much larger
items than the 42 gallon garbage bags. Preliminary
tests showed the amount of materials, plasticity of the
items (soft or hard), and preparation method (vacu-
uming to remove air in the Þlled bag before adding
CO
2
) would affect the Þnal CO
2
concentration in the
bag. Therefore, we tested the effectiveness of various
preparations (Table 2). The fabric materials included
clothing, bed sheets, pillows, mattress covers, and
socks. The boxes included cardboard and Styrofoam
boxes (total volume of the boxes in each bag was 5.9
m
3
). Two or three dishes containing bed bug eggs
(10Ð36 eggs/dish) were placed in each bag. In bags
with fabric materials only, the dishes were placed on
the top, the center, and bottom of the fabric pile. In
bags with boxes, the centerdish was placed inside
one of the boxes. Only the egg stage was tested be-
cause it was much less susceptible to CO
2
fumigation
(80% CO
2
) than nymphs and adults based on results
from Experiment 4.
After all materials were placed in each bag, a vac-
uum pump (model HB-124BS, Ho Lee Co. Ltd., Tai-
wan, Republic of China) was attached to the bag via
tubing to remove as much air as possible from the bag
(Fig. 1d). The vacuuming time lasted for 4Ð6 min.
Immediately after vacuuming, CO
2
was introduced
into the bag from a 50 lb CO
2
cylinder (Airgas East
Inc., Piscataway, NJ) via a connecting hose at 20Ð25
psi for 4Ð6 min until the bag was fully inßated. The
vacuuming/CO
2
introduction process was conducted
two times in a row in some preparations as shown in
Table 2. Repeating the vacuuming-injecting CO
2
al-
lowed for achieving higher CO
2
concentrations in the
bag. Once Þnished vacuuming and introducing CO
2
,
the hose connected to the bag was sealed with a pair
of nitrile gloves. After the desired fumigation time
(24Ð48 h) was reached, the bag was opened and the
dishes were taken out of the bags and kept in a lab-
oratory for observation of egg hatch. The temperature
of the laboratory was 22Ð24C.
Table 2. Efficacy of tanked CO
2
fumigation against bed bug eggs in Buganator plastic bags (121 183 cm)
Vacuuming/
adding CO
2
Fumigation
time (h)
Contents in
bags
Amount of materials
in each bag
No. of bags
tested
Location of bed
bugs in each bag
Mean hatch rate
(total no. of eggs)
Treated Control
Once 24 Fabric 50% full 3 Top, center 0 0% (44) 93 7% (17)
Once 25.5 Fabric 90% full 1 Top, center, bottom 42 2% (42) 100 0% (51)
Once 25.5 Fabric boxes 90% full 1 Top, center, bottom 60 3% (40) 100 0% (51)
Twice 24 Fabric 90% full 1 Top, center, bottom 1 1% (60) 89 7% (34)
Twice 24 Fabric boxes 90% full 1 Top, center, bottom 20 7% (35) 89 7% (34)
Twice 48 Fabric 50% full 1 Top, center, bottom 0 0% (69) 100 0% (50)
Twice 48 Fabric boxes 90% full 2 Top, center, bottom
a
00% (96) 100 0% (91)
Twice 72 Boxes 90% full 1 Top, center, bottom 0 0% (66) 95 3% (89)
Twice 72 Fabric boxes 90% full 1 Top, center, bottom 0 0% (72) 95 3% (89)
The room temp during the experiments was 22 to 24C.
a
The bed bug dishes at the bottomlocation were wrapped in water proof fabric.
September 2012 WANG ET AL.: CO
2
FUMIGATION FOR CONTROLLING BED BUGS 1079
Downloaded from https://academic.oup.com/jme/article-abstract/49/5/1076/1044970/Carbon-Dioxide-Fumigation-for-Controlling-Bed-Bugs
by guest
on 15 September 2017
Three 0 Ð100% CO
2
sensors were placed in each bag
to record CO
2
concentrations in bags over time (Fig.
1d). The three bags were 50, 60, and 75% full with a
mixture of fabric materials and two boxes. Each bag
was vacuumed and CO
2
was added once. Three sen-
sors were placed in each bag: at bottom of fabric pile,
inside a box on top of the fabric pile, and the center
of the fabric pile. The sensor in the center was
wrapped in water-proof fabric. The sensors recorded
CO
2
concentrations every 10 min.
To determine the Þnal CO
2
concentrations in bags
that were 90% full, three CO
2
sensors were placed in
a bag that contained a mixture of fabric materials and
boxes. The sensor locations were: bottom of clothing
pile, inside a Styrofoam box with the lid slightly open,
and inside a box. The sensor in the box was wrapped
in water-proof fabric. The bag was vacuumed and CO
2
added two times.
Data Analysis. Mortality data were corrected using
AbbottÕs (1925) formula. One-way analysis of variance
(ANOVA) was used to compare mortalities between
the treatment and the control in all experiments. All
analyses were performed using SAS software (SAS
Institute 2009).
Results
Minimum Lethal CO
2
Concentration. After 24 h
fumigation at 25C, 19.38% CO
2
did not cause signif-
icant mortality to bed bug eggs or nymphs/males (Fig.
2). The 29.86% CO
2
treatment caused signiÞcant mor-
tality to eggs (F5.52; df 2, 6; P0.044) and
nymphs/males (F12.57; df 2, 6; P0.01) with
mean corrected mortality being 12.5 4.1% for eggs
and 28.8 7.8% for nymphs/males. Thus, the mini-
mum lethal CO
2
concentration to bed bugs was 30%
when exposed for 24 h at 25C.
Relationship Between Temperature and Lethal
Time to Kill Bed Bugs by 100% CO
2
.The minimum
required time to kill 100% of test insects was negatively
correlated with temperature (Fig. 3). Eggs were al-
ways more susceptible to 100% CO
2
fumigation than
nymphs/males at the three temperatures tested. At
20C, the mean egg hatch rate was 4.2 4.2% after 7 h
fumigation. No eggs survived in 8, 9, 10, and 11 h
treatments while all eggs in the control hatched.
Nymphs/males suffered 95.6 4.4% mortality in the
12 h treatment and 100% mortality in the 14 and 15 h
treatments. There was no mortality of nymphs and
males in the control.
At 25C, one of 39 eggs hatched in the 6 h treatment.
No eggs survived in the 5, 7, 8, and 9 h treatments. The
mean hatch rate in the control was 91.7 8.3%.
Nymphs, males, and females exhibited signiÞcant mor-
tality in the 6 h treatment and nearly 100% mortality
after 8Ð10 h. One male, 1 female, and 4 nymphs
showed signs of movement after 13 h fumigation, but
did not recover. All of the insects died in the 14Ð15 h
treatments without showing any signs of movement
after being removed from the ßasks.
At 30C, only 18.3 9.8% of the eggs hatched in the
2 h 15 min treatment. No eggs hatched in the 3, 4, 5,
6, 7, and 8 h treatments. The mean egg hatch rate in
the control was 92.5 5.3%. Nymphs/males suffered
96.7 3.3% mortality in the 7 h treatment and 100%
mortality in the 8 and 9 h treatments. The mean
nymph/male mortality in the control was 1.7 1.7%.
Effect of 50 –90% CO
2
Fumigation on Bed Bugs. The
minimum exposure time required to kill 100% of
nymphs and males at 25C using 49.32 and 71.38% CO
2
were 18 and 16 h, respectively (Fig. 4). In contrast,
16 h exposure to 71.38% CO
2
only resulted in slightly
lower egg hatch rate (83.0 1.7%) compared with the
control (97.8 2.2%) (F25.5; df 1, 4; P0.01).
Using 24 h treatment time and higher CO
2
concen-
trations at 30C resulted in higher egg mortality. The
mean corrected mortality in 78.96 and 89.64% CO
2
treatments were 75.6 12.3 and 100 0%, respec-
tively (Fig. 5). No additional eggs hatched after 11 d.
The mean egg hatch rate in the control was 93.9
3.3%.
Efficacy of CO
2
Fumigation in Heavy-Duty Gar-
bage Bags. In the test using 900 g dry ice per bag, all
eggs were killed. The mean egg hatch rate in the
control was 98.1 1.9%. Three males (30%) and 6
nymphs (60%) located at the toplocation in one
treated bag survived. The mean nymph/male mortal-
ity in the control was 3.9 2.0%.
Fig. 2. Effect of 24 h exposure to elevated CO
2
levels on
bed bug eggs (mean % hatch and SEM) at 25C.
Fig. 3. Relationship between temperature and lethal
time to kill bed bugs by 100% CO
2
. The maximum time
required to kill all tested insects in the three replicates is
shown.
1080 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 49, no. 5
Downloaded from https://academic.oup.com/jme/article-abstract/49/5/1076/1044970/Carbon-Dioxide-Fumigation-for-Controlling-Bed-Bugs
by guest
on 15 September 2017
All eggs, nymphs, and males died in the 1,350 g dry
ice treated bags. Bed bug nymphs and males showed
no signs of movement after the 24 h fumigation treat-
ment. The mean egg hatch rate in the control was
94.6 4.7%. The mean nymph/male mortality in the
control was 1.7 1.7%.
CO
2
sensors in each bag recorded similar peak levels
of CO
2
, with the top location reaching the peak con-
centration at the slowest speed (Fig. 6). The average
CO
2
concentrations within each bag plateaued at 5
h and were maintained at 94% after 24 h.
Efficacy of CO
2
Fumigation in Custom-Made Fu-
migation Bags. All bed bug eggs were killed after 24 h
fumigation when each bag was vacuumed, CO
2
was
introduced once, and the bag was 50% full of materials
(Table 2). When the bags were 90% full, it required
the bags to be vacuumed and injected with CO
2
two
times, and a 48 h fumigation period to successfully kill
all bed bug eggs.
When vacuumed and CO
2
was introduced once, it
took 190, 210, and 310 min, respectively, to reach stable
CO
2
concentrations in the center of the Buganator
bags Þlled 50, 75, and 90% with fabric materials (Fig.
7). The Þnal CO
2
concentration was negatively cor-
related with the volume of the bag contents. Each
Buganator bag was able to keep constant, high CO
2
concentrations. In a bag 90% full of fabric materials,
cardboard boxes, and Styrofoam boxes, the mean Þnal
CO
2
concentration measured was 66 2% (Fig. 8).
Wrapping the CO
2
sensor tightly inside water proof
fabric slowed down CO
2
penetration, but only slightly
reduced the Þnal CO
2
concentration.
Discussion
We showed that using dry ice or tanked CO
2
and
thick plastic bags can effectively kill bed bugs hidden
in household items after 24 or 48 h treatment at room
temperature. The minimum required time to kill 100%
of bed bugs is affected by the room temperature,
amount of materials placed in a bag, and quantity of
CO
2
introduced into each bag. It is also possible the
physiological status of the bed bugs (such as nutri-
tional status, days after molting) may affect the bed
bug susceptibility to CO
2
fumigation. We did not try
to control the exact age of the bed bugs or feeding
status of the bed bugs when conducting the experi-
ments. This may have resulted in large variances and
irregular time-mortality response patterns.
Eggs were more susceptible to 100% CO
2
than mo-
bile stages but much less susceptible than mobile
stages at 50Ð80% CO
2
concentrations. Although we
did not test females using 50Ð80% CO
2
concentra-
tions, it is predicted that females will have similar
mortality response as males and nymphs as shown in
Fig. 6. Mean CO
2
concentration in heavy-duty garbage
bags that were 90% full. In total, 1,350 g of dry ice pellets were
placed near the bottom, the center, and near the top of the
contents in each bag. Three CO
2
sensors were placed in each
bag.
Fig. 4. Effect of CO
2
fumigation on bed bug mortality (mean SEM) of nymphs and adult males: (A) 49.32% CO
2
; (B)
71.31% CO
2
.
Fig. 5. Effect of 78.96% CO
2
fumigation on bed bug eggs
(mean % hatch and SEM) at 25C.
September 2012 WANG ET AL.: CO
2
FUMIGATION FOR CONTROLLING BED BUGS 1081
Downloaded from https://academic.oup.com/jme/article-abstract/49/5/1076/1044970/Carbon-Dioxide-Fumigation-for-Controlling-Bed-Bugs
by guest
on 15 September 2017
the 100% CO
2
treatment. The higher sensitivity to
100% CO
2
in eggs is interesting. Presumably, insect
eggs have lower metabolism rate than the mobile
stages and is the most tolerant stage regardless of the
CO
2
concentration being used (Riudavets et al. 2010).
The different relative susceptibility to various CO
2
levels suggests modiÞed air with 0% oxygen is more
lethal to eggs than the mobile stages. However, when
low level oxygen is present, eggs can survive better
than nymphs and adults.
Compared with other insects studied, bed bugs are
more sensitive to CO
2
fumigation than Formosan sub-
terranean termite (Coptotermes formosanus Shiraki)
(Delate et al. 1995), Oriental cockroach (Blatta ori-
entalis L.) (Gannon et al. 2001), German cockroach
(Blattella germanica (L.) (C.W., unpublished data),
red ßour beetle (Tribolium castaneum (Herbst)) (Bai-
ley and Banks 1975), rusty grain beetle (Cryptolestes
ferrugeneius (Stephens)) (Mann et al. 1999), and sev-
eral other stored product pests (Annis 1987). The
relatively short required fumigation time (1Ð2 d)
makes CO
2
fumigation a promising technique for elim-
inating bed bugs from infested household items. The
materials and procedures involved in CO
2
fumigation
are relatively simple and inexpensive. Larger sizes of
Buganator bags are available for treating large house-
hold items such as sofas or mattresses. The Buganator
bags were able to maintain a constant high CO
2
con-
centration throughout the fumigation period without
the need for adding CO
2
during fumigation. Sealed
garbage bags were not as air tight as the Buganator
bags. However, when a large enough amount of dry ice
was placed in each garbage bag, high concentrations
of CO
2
(94%) were maintained for at least 24 h,
which is sufÞcient for complete control of bed bugs at
room temperature.
The required CO
2
fumigation time to kill 100% of
bed bugs was negatively correlated with the environ-
mental temperature and negatively correlated with
the CO
2
concentration in the bags. We tested under
the most challenging conditions where each fumiga-
tion bag was 90% full and both soft, hard, and water
proof materials were included. CO
2
sensors wrapped
in water proof fabric recorded similar Þnal CO
2
con-
centration as those nonwrapped sensors, indicating
water proof materials can be effectively treated, but
will require longer fumigation time than nonwater
proof fabric materials.
When a smaller volume of material is placed in each
Buganator bag, bed bugs may be killed faster because
higher CO
2
concentration can be achieved. In envi-
ronments where the temperature is lower than 23C,
a heating fan can be placed inside the Buganator bag
to maintain a warm temperature. Each Buganator bag
is equipped with a reattachable power cable that can
be connected to one of the round openings. We placed
a fan heater (model FH03D, Ningbo Dongji Elec-
tronic Technology, Co., China) in a Buganator bag
that was 70% full of boxes and a few pieces of fabric.
The heating fan increased the temperature inside the
bag by at least 12C. In a bag that was 80% full of fabric
materials, the heating fan increased the temperature
by at least 4C. Larger volumes of tightly packed fabric
materials were more difÞcult to warm up than rigid
materials (e.g., boxes).
Fig. 7. CO
2
concentration measured at the center of
Buganator bags that were Þlled with different amounts of
fabric materials. The bag was vacuumed and injected with
CO
2
once. The CO
2
sensor was wrapped inside a piece of
water proof fabric.
Fig. 8. CO
2
concentration measured at different locations within a bag Þlled 90% full with fabric materials and boxes. The
bag was vacuumed and injected twice with CO
2
from a CO
2
cylinder.
1082 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 49, no. 5
Downloaded from https://academic.oup.com/jme/article-abstract/49/5/1076/1044970/Carbon-Dioxide-Fumigation-for-Controlling-Bed-Bugs
by guest
on 15 September 2017
Potential risks of CO
2
fumigation using dry ice or
tanked CO
2
include injury from direct contact with
dry ice and increased CO
2
levels when adding dry ice
or tanked CO
2
into bags or during aeration after fu-
migation. The risk of asphyxiation can occur when
many garbage bags are used in a small room. Trans-
porting dry ice or CO
2
cylinders may also present
safety risks. These risks can be easily prevented by
wearing gloves, ventilating the rooms during fumiga-
tion, and ventilating the vehicle when transporting dry
ice. It is recommended that individuals who want to
use this technique obtain proper training to ensure
safe and effective use of the technique. CO
2
fumiga-
tion should not be used as a whole house treatment
because it is very difÞcult, if not impossible, to reach
lethal CO
2
concentration for extended period of time
that is necessary to kill all bed bug stages. It should also
be noted that releasing CO
2
into the atmosphere con-
tributes to the green house effect. Nevertheless, com-
pared with other treatment methods currently used
for treating bed bug-infested household items, CO
2
fumigation is unlikely to damage the treated items,
very inexpensive, and leaves no residue.
In conclusion, CO
2
fumigation in plastic containers
offers an effective, affordable, and fast way to treat bed
bug-infested household items, many of which cannot
be treated readily by other techniques. It can be used
as part of an integrated bed bug management program.
The fumigation process may increase the CO
2
levels in
a closed room to an injurious level. Proper ventilation,
especially during the introduction of CO
2
and venti-
lation of the bag, is required to prevent the risk of
accidental asphyxiation.
Acknowledgments
We thank Marcus Kwasek, Moneen Jones, and Vincenzo
Averello for technical assistance. Susan McKnight provided
suggestions on using dry ice as a fumigation tool. Protect-A-
Bed and U.S. Department of Agriculture Northeastern Inte-
grated Pest Management Center provided funding for this
project. Kurt Saltzmann and Richard Cooper reviewed an
earlier draft of this paper. This is New Jersey Experiment
Station Publication D-08-08117-01-12.
References Cited
Abbott, W. S. 1925. A method of computing the effective-
ness of an insecticide. J. Econ. Entomol. 18: 265Ð267.
Adler, C., H. G. Corinth, and C. Reichmuth. 2000. ModiÞed
atmospheres, pp. 105Ð146. In Bh. Subramanyam and D. W.
Hagstrum (eds.), Alternatives to Pesticides in Stored
Product IPM. Kluwer Academic Publishers, Boston, MA.
Annis, P. C. 1987. Towards rational controlled atmosphere
dosage schedules: a review of current knowledge, pp.
128 Ð148. In E. Donahaye and S. Navarro (eds.), Proceed-
ings, 4th International Working Conference on Stored-
Product Protection, 21Ð26 September 1986, Tel Aviv, Is-
rael.
Bailey, S. W., and H. J. Banks. 1975. The use of controlled
atmospheres for the storage of grain, pp. 362Ð374. In E. U.
Brady, J. H. Brower, P. E. Hunter, E. G. Jay, P.T.M. Lum,
H. O. Lund, M. A. Mullen, and R. Davis (eds.), Proceed-
ings, 1st International Working Conference on Stored-
Product Entomology, 7Ð11 October 1974, Savannah, GA.
Delate, K. M., J. K. Grace, J. W. Armstrong, and C.H.M.
Tome. 1995. Carbon dioxide as a potential fumigant for
termite control. Pest Manag. Sci. 44: 357Ð461.
Doggett, S. 2011. A code of practice for the control of bed
bug infestations in Australia, 4th ed. (http://medent.
usyd.edu.au/bedbug/bedbug_cop.htm).
Gannon, B., G. Le Patourel, and R. Young. 2001. Effect of
carbon dioxide on the Oriental cockroach, Blatta orien-
talis. Med. Vet. Entomol. 15: 68Ð72.
Hayes, W. J., and E. R. Laws (ed.). 1990. Handbook of pes-
ticide toxicology, vol. 3, Classes of Pesticides. Academic,
Inc., New York, NY.
Herrmann, J., C. Adler, G. Hoffmann, and C. Reichmuth.
1999. EfÞcacy of controlled atmospheres on Cimex lectu-
larius (L.) (Heteroptera: Cimicidae) and Argas reflexus
Fab. (Acari: Argasidae), p. 637. In W. H. Robinson, F.
Rettich, and G. W. Rambo (eds.), Proceedings of the 3rd
International Conference on Urban Pests, 19Ð22 July
1999, Prague, Czech Republic.
Lehnert, M. P., R. M. Pereira, P. G. Koehler, W. Walker, and
M. S. Lehnert. 2011. Control of Cimex lectularius using
heat combined with dichlorvos resin strips. Med. Vet.
Entomol. 25: 460Ð464.
Mann, D. D., D. S. Jayas, W. E. Muir, and N.D.G. White.
1999. EfÞcient carbon dioxide fumigation of wheat in
welded-steel hopper bins. Appl. Eng. in Agric. 15: 57Ð63.
Navarro, S. 2006. ModiÞed atmospheres for the control of
stored product insects and mites, pp. 105Ð145. In J. W.
Heaps (ed.), Insect Management for Food Storage and
Processing. AACC International, St. Paul, MN.
Navarro, S., B. Timlick, C. J. Demianyk, and N.D.G. White.
2012. Chapter 16: controlled and modiÞed atmospheres,
25 pp. In D. W. Hagstrum, T. W. Phillips, and G. Cuperus
(eds.), Stored Product Protection. Kansas State Univer-
sity Research and Extension Publication S156.
Nicolas, G., and D. Sillans. 1989. Immediate and latent ef-
fects of carbon dioxide on insects. Annu. Rev. Entomol.
34: 97Ð116.
Riudavets, J., C. Castan˜e´, O. Alomar, M. J. Pons, and R.
Gabarra. 2009. ModiÞed Atmosphere Packaging (MAP)
as an alternative measure for controlling ten pests that
attack processed food products. J. Stored Prod. Res. 45:
91Ð96.
Romero, A., M. F. Potter, D. A. Potter, and K. F. Haynes.
2007. Insecticide resistance in the bed bug: a factor in the
pestÕs sudden resurgence? J. Med. Entomol. 44: 175Ð178.
SAS Institute. 2009. SAS/STAT userÕs guide, version 9.2.
SAS Institute, Cary, NC.
Zhu, F., J. Wigginton, A. Romero, A. Moore, K. Ferguson, R.
Palli, M. F. Potter, K. F. Haynes, and S. R. Palli. 2010.
Widespread distribution of knockdown resistance muta-
tions in the bed bug, Cimex lectularius (Hemiptera: Cimi-
cidae), populations in the United States. Arch. Insect
Biochem. Physiol. 73: 245Ð257.
Received 21 February 2012; accepted 28 June 2012.
September 2012 WANG ET AL.: CO
2
FUMIGATION FOR CONTROLLING BED BUGS 1083
Downloaded from https://academic.oup.com/jme/article-abstract/49/5/1076/1044970/Carbon-Dioxide-Fumigation-for-Controlling-Bed-Bugs
by guest
on 15 September 2017
... [2][3][4][5][6] A multifaceted approach such as integrated pest management (IPM), which includes rational use of pesticides along with frequent monitoring and use of different alternative control measures, has proven effective for their control. 7,8 In addition to a plethora of insecticide efficacy reports, several studies have demonstrated and/or tested the effectiveness of alternative control methods such as heat treatments, 9 cold treatments, 10 steam, 11,12 desiccant dusts, 13 carbon dioxide and dry ice, 14,15 ultra-low oxygen and vacuum treatments, 16 insecticide-treated mattress encasements, 17 essential oils 18,19 and fumigants 20,21 for C. lectularius control. Unlike published reports on insecticide and alternative control techniques, only one preliminary study has assessed the ability of ozone (O 3 ) gas to kill C. lectularius adults; 22 the remainder of the non-empirical information on the efficacy of ozone can be found online (https://www.foreverozone.com/ ...
... Although the specific causes of species-dependent variation in the insecticidal activity of ozone remain unknown, they may be caused by differences in body mass, respiration rate and/or oxidative stress response mechanisms, which likely vary between different groups and species of pest insects. 52,53 In comparison with the ozone CT product (270 000 ppm-min) required to achieve 100% mortality of insecticide-susceptible C. lectularius nymphs and adults, the minimum carbon dioxide concentration required to kill all mobile life stages of a field strain of C. lectularius was 30% or 300 000 ppm with an exposure time of 24 h or 1440 min, 14 which translates to a CT product of 432 000 000 ppm-min. ...
... Commercially available ozone sensors can be used by pest management professionals to monitor ozone concentrations during and after treatment. Interestingly, safety and waiting standards for using carbon dioxide fumigation for C. lectularius control 14 are not currently regulated by the EPA. However, regulations for pests such as beetles, lice and moths indicate that carbon dioxide concentrations in work areas cannot exceed 0.5% or 5000 pm (https:// www.fsis.usda.gov/wps/wcm/connect/bf97edac-77be-4442-aea4-9d2615f376e0/Carbon-Dioxide.pdf?MOD=AJPERES). ...
Article
BACKGROUND Ozone gas is commercially used for deodorization and microbial control. Its efficacy against stored product insect pests is well documented. In the midst of the common bed bug (Cimex lectularius L.) outbreak, claims were made that ozone gas was effective for their control. This study was conducted to determine baseline ozone concentrations and exposure times required for the control of an insecticide susceptible C. lectularius strain under laboratory conditions. Dichlorvos (DDVP), an organophosphate class fumigant insecticide was used as a positive control. RESULTS Nymphs and adults were more susceptible to ozone than eggs. Complete (100%) nymph and adult mortality was achieved at ozone concentration (C) of 1500 ppm and exposure time (T) of 180 min or CT product of 270 000 ppm‐min, whereas eggs required an 8 fold higher CT (2 040 000 ppm‐min). Vapors of DDVP were 2070, 2542 and 450 fold more potent than ozone, against nymphs, adults and eggs, respectively. CONCLUSIONS Baseline ozone toxicity data provide insights on the practicality of using this gas for management of common bed bugs. High ozone CT products required for C. lectularius control, particularly for eggs, suggests that its use for treating infested human dwellings is not feasible due to logistic, safety and monetary concerns.
... [2][3][4][5][6] A multifaceted approach such as integrated pest management (IPM), which includes rational use of pesticides along with frequent monitoring and use of different alternative control measures, has proven effective for their control. 7,8 In addition to a plethora of insecticide efficacy reports, several studies have demonstrated and/or tested the effectiveness of alternative control methods such as heat treatments, 9 cold treatments, 10 steam, 11,12 desiccant dusts, 13 carbon dioxide and dry ice, 14,15 ultra-low oxygen and vacuum treatments, 16 insecticide-treated mattress encasements, 17 essential oils 18,19 and fumigants 20,21 for C. lectularius control. Unlike published reports on insecticide and alternative control techniques, only one preliminary study has assessed the ability of ozone (O 3 ) gas to kill C. lectularius adults; 22 the remainder of the non-empirical information on the efficacy of ozone can be found online (https://www.foreverozone.com/ ...
... Although the specific causes of species-dependent variation in the insecticidal activity of ozone remain unknown, they may be caused by differences in body mass, respiration rate and/or oxidative stress response mechanisms, which likely vary between different groups and species of pest insects. 52,53 In comparison with the ozone CT product (270 000 ppm-min) required to achieve 100% mortality of insecticide-susceptible C. lectularius nymphs and adults, the minimum carbon dioxide concentration required to kill all mobile life stages of a field strain of C. lectularius was 30% or 300 000 ppm with an exposure time of 24 h or 1440 min, 14 which translates to a CT product of 432 000 000 ppm-min. ...
... Commercially available ozone sensors can be used by pest management professionals to monitor ozone concentrations during and after treatment. Interestingly, safety and waiting standards for using carbon dioxide fumigation for C. lectularius control 14 are not currently regulated by the EPA. However, regulations for pests such as beetles, lice and moths indicate that carbon dioxide concentrations in work areas cannot exceed 0.5% or 5000 pm (https:// www.fsis.usda.gov/wps/wcm/connect/bf97edac-77be-4442-aea4-9d2615f376e0/Carbon-Dioxide.pdf?MOD=AJPERES). ...
Article
BACKGROUND Ozone gas is commercially used for deodorization and microbial control. Its efficacy against stored product insect pests is well documented. In the midst of the common bed bug (Cimex lectularius L.) outbreak, claims were made that ozone gas was effective for their control. This study was conducted to determine baseline ozone concentrations and exposure times required for the control of an insecticide susceptible C. lectularius strain under laboratory conditions. Dichlorvos (DDVP), an organophosphate class fumigant insecticide was used as a positive control. RESULTS Nymphs and adults were more susceptible to ozone than eggs. Complete (100%) nymph and adult mortality was achieved at ozone concentration (C) of 1500 ppm and exposure time (T) of 180 min or CT product of 270 000 ppm‐min, whereas eggs required an 8 fold higher CT (2 040 000 ppm‐min). Vapors of DDVP were 2070, 2542 and 450 fold more potent than ozone, against nymphs, adults and eggs, respectively. CONCLUSIONS Baseline ozone toxicity data provide insights on the practicality of using this gas for management of common bed bugs. High ozone CT products required for C. lectularius control, particularly for eggs, suggests that its use for treating infested human dwellings is not feasible due to logistic, safety and monetary concerns. This article is protected by copyright. All rights reserved.
... [2][3][4][5][6] A multifaceted approach such as integrated pest management (IPM), which includes rational use of pesticides along with frequent monitoring and use of different alternative control measures, has proven effective for their control. 7,8 In addition to a plethora of insecticide efficacy reports, several studies have demonstrated and/or tested the effectiveness of alternative control methods such as heat treatments, 9 cold treatments, 10 steam, 11,12 desiccant dusts, 13 carbon dioxide and dry ice, 14,15 ultra-low oxygen and vacuum treatments, 16 insecticide-treated mattress encasements, 17 essential oils 18,19 and fumigants 20,21 for C. lectularius control. Unlike published reports on insecticide and alternative control techniques, only one preliminary study has assessed the ability of ozone (O 3 ) gas to kill C. lectularius adults; 22 the remainder of the non-empirical information on the efficacy of ozone can be found online (https://www.foreverozone.com/ ...
... Although the specific causes of species-dependent variation in the insecticidal activity of ozone remain unknown, they may be caused by differences in body mass, respiration rate and/or oxidative stress response mechanisms, which likely vary between different groups and species of pest insects. 52,53 In comparison with the ozone CT product (270 000 ppm-min) required to achieve 100% mortality of insecticide-susceptible C. lectularius nymphs and adults, the minimum carbon dioxide concentration required to kill all mobile life stages of a field strain of C. lectularius was 30% or 300 000 ppm with an exposure time of 24 h or 1440 min, 14 which translates to a CT product of 432 000 000 ppm-min. ...
... Commercially available ozone sensors can be used by pest management professionals to monitor ozone concentrations during and after treatment. Interestingly, safety and waiting standards for using carbon dioxide fumigation for C. lectularius control 14 are not currently regulated by the EPA. However, regulations for pests such as beetles, lice and moths indicate that carbon dioxide concentrations in work areas cannot exceed 0.5% or 5000 pm (https:// www.fsis.usda.gov/wps/wcm/connect/bf97edac-77be-4442-aea4-9d2615f376e0/Carbon-Dioxide.pdf?MOD=AJPERES). ...
... Poisonous gases, such as sulfuryl fluoride (Miller and Fisher, 2008;Phillips et al., 2014) and methyl bromide, and inert gases, such as carbon dioxide and ozone (Wang et al., 2012;Martin and Henderson, 2013;Nanoudon and Chanbang, 2014;Feston, 2015) have been used as fumigants for the control of bed bugs. Poisonous gases have the great advantage of potentially being able to penetrate deep into all the hidden areas and harborages of the insect, and can kill eggs and all bed bug stages. ...
... Unlike poisonous gases, the penetration ability of most inert gases is poor and would require a longer period to reduce the bed bug population. Carbon dioxide is an exception, and has been shown to be able to penetrate dense material easily (Wang et al., 2012). ...
... Also used have been Petri dishes (Choe and Campbell, 2014;Feldlaufer and Ulrich, 2015) and 15 × 15 cm ceramic tiles (How and Lee, 2011). Evaluation has also been undertaken in plastic garbage bags when evaluating volatile compounds (Wang et al., 2012;Feldlaufer and Ulrich, 2015). It is presently unknown if arena size affects efficacy. ...
Chapter
In a survey of pest management professionals, bed bugs were ranked as the most difficult of all urban pests to control, largely due to issues of insecticide resistance. Successful bed bug management relies on integrated pest management, encompassing non‐chemical means of control, as well as the judicious use of insecticides. Despite the resistance issues, chemicals are often necessary to completely eradicate an infestation. Using the right insecticide in the correct formulation is crucial for successful bed bug management. Throughout history, there have been a number of insecticide classes used against bed bugs. However, some of the most effective insecticides are no longer permitted for use due to environmental and human safety concerns. To date, the majority of insecticide efficacy evaluations have been undertaken on the Common bed bug, Cimex lectularius L., with only a limited number of trials on the Tropical bed bug, Cimex hemipterus (F.). The published evaluations on C. lectularius have mostly been undertaken in the USA, while the majority of those on C. hemipterus were completed in Africa, and more recently, in Thailand and Malaysia. This chapter reviews the literature on chemical control relevant to the modern bed bug resurgence, namely from 1990 to early 2017, focusing on insecticidal classes that are in common use today.
... Among the tested stages of D. suzukii, eggs were the most tolerant life stage to EF fumigation, at both 5 and 21 • C. Eggs are generally the most tolerant life stage of insects to many fumigants (Armstrong and Whitehand, 2005;Wang et al., 2012) and our results with EF are in agreement with studies conducted on other species of insect (Jamieson et al., 2015;Bessi et al., 2015;Lee et al., 2018;Park et al., 2020). In contrast, the third instar larvae of D. suzukii were most tolerant when infested strawberries were treated using MB at 18 • C (Walse et al., 2012). ...
Article
Spotted wing drosophila, Drosophila suzukii (Diptera: Drosophilidae), is a serious invasive pest of berries and cherries in the U.S. and Europe and has become a major phytosanitary trade barrier. In this pilot study, we explored the potential of using stand-alone ethyl formate (EF) treatment and a combinatory treatment of EF and cold temperature as postharvest control options for D. suzukii in imported blueberries. Stand-alone EF fumigations were effective against D. suzukii with LCt99% of 207.7 and 168.5 g·h·m⁻³ for eggs, the most tolerant life stage, at 5 and 21 °C, respectively. In a scale-up (10 m³) trial conducted at 5 °C, complete control of D. suzukii eggs placed inside and outside of blueberry boxes was achieved using 70 g·m⁻³ EF for 4 h with 5% blueberry loading ratio without deleterious impact on blueberry appearance such as soft spot or berry shrivel. In small scale pilot studies, 9-d stand-alone cold treatment at 5 °C was sufficient for complete control of D. suzukii eggs and larvae tested, but not pupae. The efficacy of this cold treatment appeared to be improved when D. suzukii eggs were first treated with low-dose EF (LCt50% level) prior to the cold treatment. The combination treatment resulted in complete mortality of D. suzukii eggs, larvae, and pupae tested after 7, 5, and 9 d of cold treatment, respectively. Together, these results suggest that stand-alone EF treatment, or the combination treatment of low-dose EF and cold as a systems approach may have a potential as postharvest treatments for D. suzukii in blueberries.
... Meningkatnya konsentrasi CO₂ dalam ruang kedap udara akan menyebabkan kematian serangga hama ( Noomhorm et al. 2013). Changlu et al. (2012) menambahkan, kematian serangga hama disebabkan kadar CO₂ yang meningkat menyebabkan spirekel serangga tetap terbuka, sehingga serangga mengalami dehidrasi. ...
Article
Full-text available
Cylas formicarius is the main pest of sweet potatoes especially in storage. Damage from the pest attacks can reduce yields up to 97% and even minor damage causes sweet potatoes cannot be consumed because they taste bitter and toxic. Warehouse pest control such as C. formicarius is generally carried out by fumigation. Dry ice is a solid CO₂ that can be used as a fumigant to control warehouse pests. This study aims to determine the application of dry ice as fumigant and different storage places for C. formicaius in sweet potatoes. The variables observed C. formicarius population and mortality, weight loss, decrease in water content, level of damage to sweet potatoes and taste testing. The results showed that the population of C. formicarius in control higher than the other treatments, in the storage area in the population space C. formicarius is higher than in dark storage. Mortality in the treatment of giving dry ice reached 100% at the dose of 5g, 10g and 15g. Weight reduction and decrease in water content in sweet potatoes correlate with each other where in the control treatment changes in weight and water content are highest compared to other treatments. Storage places have no effect on weight loss and loss of water content in sweet potatoes. Taste of sweet potatoes before and after the shelf life with the dry ice application has not changed.
... Carbon dioxide exposure might affect insect longevity, mating success and growth, feeding, development, reproduction, and behavior ( Bartholomew et al., 2015). With a 24-h exposure time at 25 °C, a lethal concentration of CO 2 for all bed bugs stages was approximately 30% ( Wang et al., 2014). The use of high CO 2 concentrations in gastight large bags is a possible method for preventing the occurrence of post-harvest pests on agricultural commodities, including rice, cocoa, beans, and various dried herbs during storage ( Pons et al., 2010). ...
Article
In Thailand, lotus flowers are one of exportable products for flower trade industry. Common blossom thrip (Frankliniella schultzei) contamination on cut lotus flowers after harvest has been a major problem for export. F. schultzei is a quarantine insect pest. Modified atmospheres (MA) without oxygen content are considered an alternative to methyl bromide fumigation to control thrips. MA treatment has been used to control insect pests in agricultural product commodities. Different combinations of carbon dioxide, nitrogen, ozone levels, and treatment times were used to effect mortality of the common blossom thrips and postharvest quality of cut lotus flowers. Exposure to different concentrations of O3 fumigation for 2 days could kill almost all F. schultzei (100% of larvae and ≥ 96% of adults). However, a concentration of 50-250 ppm of O3 could not control F. schultzei on lotus flowers completely. O3 fumigation caused color change in lotus flowers. High concentrations of O3 (≥ 150 ppm) had a negative effect on the visual quality of lotus flowers. The results revealed that thrips mortality increased with increased CO2 level and storage time. 100% CO2 caused 100% mortality of both adults and larvae of F. schultzei when there was a 6-h exposure. MA were more effective in disinfecting of thrips on cut lotus flowers after 9 h fumigation to ≥ 50% CO2 caused complete mortality to F. schultzei. There was not much difference in lotus color in response to atmosphere modified by a combination of CO2 and N2. Therefore, CO2 disinfestation treatment has the potential to be developed commercially as an alternative postharvest control for common blossom thrips on lotus flowers.
... The latter system has been commercially available for some years and can be used to control bed bugs on mattresses, but some days are required to achieve a complete kill. Carbon dioxide via dry ice or compressed gas can also be added to containers that are subsequently sealed to kill bed bugs within (Wang et al. 2012). Clearly such systems are aimed at small-scale treatments due to the logistics involved in bagging and sealing infested items, in particular the treatment of sensitive objects such as electronic devices, which heating or freezing may damage. ...
Chapter
The global resurgence of bed bugs has been well‐documented in the literature and has been extremely costly to society. In the USA alone, revenue derived by pest management companies related to bed bug infestations rose to USD 611.2 million in 2016. It stands to reason that the two key aspects in mitigating the impact of the Common bed bug, Cimex lectularius L., and the Tropical bed bug, Cimex hemipterus (F.), revolve around: Detection: Is a bed bug infestation actually present? Control: What is the best way to eliminate a bed bug infestation? In spite of the advances in detection and the control of bed bugs, certain limitations still exist in bed bug management technologies. This chapter attempts to address many of these limitations, and to critically review the potential of current and proposed bed bug management technologies.
Article
Full-text available
Formosan subterranean termites, Coptotermes formosanus Shiraki, were exposed to ⩾ 95% or 50% carbon dioxide atmospheres for intervals of 24-120 h at 26(±3)°C. A 24-h exposure to ⩾ 95% carbon dioxide caused significant termite mortality, but 60 h were required for complete mortality. Exposure to 50% carbon dioxide for 60 h resulted in approximately 70% termite mortality, while complete mortality was recorded after 120 h. When termites were sealed in wooden blocks (90 × 90 × 152 mm), 72-96 h exposure to ⩾ 95% carbon dioxide was necessary for complete control. A limited study with Cryptotermes brevis (Walker) suggested that this drywood termite is also susceptible to carbon dioxide fumigation, although slightly longer exposures may be required than with C. formosanus. Carbon dioxide-modified atmospheres are a viable alternative to conventional fumigants for vault fumigation of termite-infested materials, and may also be applicable to larger-scale fumigations to control structural pests.
Article
Two welded-steel hopper bins were modified for fumigation with carbon dioxide (CO2) and a method for efficiently purging the air from the bins was developed. Concentrations of CO2 during experimental fumigations were less than the concentrations predicted theoretically, but were high enough to kill more than 99% of caged adult rusty grain beetles in three separate experiments. Between 58 and 75% of the CO2 initially added remained in the bin at the time when the CO2 concentrations peaked. The positive results from this research mean that stored-product insects in stored grain can be controlled using CO2 rather than continuing to rely on synthetic insecticides and fumigants that present health and environmental concerns.
Article
Les actions du CO 2 sont variees et ont lieu a differents niveaux. On connait peu de choses des mecanismes de perception du CO 2 et la transmission initiant des reponses. Des effets au niveau cerebral, endocrinologique, metabolique, respiratoire et circulatoire ont ete mis en evidence mais aucune explication unifiee des consequences comportementales et biologiques ne peut etre fournie. L'utilisation du CO 2 comme anesthesiant devrait etre limite en absence d'analyse precise de ses effets.
Article
Modified atmospheres based on high carbon dioxide (CO2) content offer an alternative to fumigation for arthropod pest control in durable commodities. The present study aimed to establish the efficacy of using modified atmospheres during packaging (MAP) to control a wide spectrum of pests and their respective developmental stages that affect final food products during storage and commercialization. Two high (50% and 90%) CO2 MAPs were applied to identify the pest species and developmental stages that were most tolerant to treatments. Standard food diets containing eggs, larvae, pupae and adults of Lasioderma serricorne, Cryptolestes ferrugineus, Oryzaephilus surinamensis, Tribolium confusum, Rhyzopertha dominica, Sitophilus oryzae, Ephestia kuehniella, Plodia interpunctella, Liposcelis bostrychophila and Tyrophagus putrescentiae were confined in sealed plastic bags filled with the two MAPs. The pest species and developmental stages showed different sensitivity to the two MAP treatments. The beetles S. oryzae, R. dominica, C. ferrugineus and L. serricorne were among the most tolerant species as pupae or eggs. The mite T. putrescentiae was also highly tolerant. Moths were easier to kill than the other species tested. Our results confirmed that MAP could be applied to final food products during packaging to control the residual occurrence of pests after the manufacturing process and to prevent further infestation in the final packages reaching consumers.