High Resistance of
Pyrethroid-Resistant Blattella germanica
(Dictyoptera: Blattellidae) Population of Palembang Disassociated with Cuticle
Thickening Mechanism
Resti Rahayu*, Vivy Hermana Pratiwi and Kamsiah Wulan Purnama Sari
Department of Biology, Faculty of Mathematics and Natural Sciences,
Universitas Andalas, 25163, Padang, West Sumatera, Indonesia
*For correspondence: restirahayu@sci.unand.ac.id
Received 20 December 2023; Accepted 04 March
2024; Published 16 April 2024
Abstract
Blattella germanica L. is highly adaptive to the human environment and
reportedly resistant to extensive insecticides. Pyrethroid aerosol is
predominantly used to control this pest in households causing more resistance.
Reduced insecticide penetration has been reported in B. germanica since the
1960s, allowing for cuticle modification in resistant individuals. This study
aimed to determine the resistance ratio of cockroaches to six pyrethroid
aerosol insecticides in Indonesia (By, Ht, Vp, Fm, Mt, Nm) and detect the
presence of cuticle thickening mechanism in pyrethroid-resistant B. germanica. This study used the
PLZ-PLM strain, originating from Palembang as a field strain, and VCRU-WHO
(Vector Control Research Unit-WHO) as a standard strain. The result showed that
the resistance ratio of the PLZ-PLM strain to the six aerosol insecticides was
18–45 fold, which confirmed that the PLZ-PLM was highly resistant to all the
aerosol insecticides used. There was no significant difference in the average
cuticle thickness between resistant PLZ-PLM cockroaches and strains susceptible
to pyrethroids (Mann Whitney U-Test, Z= -0.731, P < 0.05). The absence of a cuticle thickening in
pyrethroid-resistant PLZ-PLM strain indicates that other mechanisms contribute
to the resistance. This study illustrates the need to evaluate the use of
aerosol insecticides in controlling B.
germanica. Also, the result confirms that cuticle thickening plays a minor
role in the insecticide resistance mechanism. © 2024
Friends Science Publishers
Keywords: Aerosol; Blattella
germanica L.; Cuticle thickness; Insecticide resistance;
Pyrethroid
Introduction
Blattella germanica L., commonly known as the German cockroach, is the most
common pest cockroach found in residential areas (Bell et al. 2007) and is included in the top 6 urban insect pests (Zhu et al. 2016). Population control is of
concern because of its negative impact on human health (Pérez 1989) and its
very high adaptive capacity to various environmental conditions (Bell et al. 2007). Until now, insecticides have
been the key to controlling B. germanica,
but their widespread and excessive use has increased resistance, failing to
control this species (Wu and Appel 2017). Since the 1950s, B. germanica has been reported to be resistant to
dichlorodiphenyltrichloroethane (DDT) (Cochran
et al. 1953), which then has extended
to 45 types of insecticides (Arthropod Pesticide Resistance Database, 2023). In
Indonesia, cases of German cockroach resistance to several insecticides have
also been reported (Ahmad et al.
2009; Rahayu et al. 2012; Rahayu et al. 2016; Nurseha et al. 2019).
Pyrethroids
have been commonly used for German cockroach control in recent years due to
their low toxicity to mammals (Shiravand et
al. 2018). In common, this insecticide is commercially formulated as an
aerosol passing around the community. Unfortunately, studies have found that
some aerosol insecticides are no longer effective in killing German cockroaches
in Indonesia (Rahayu et al. 2016;
Rahayu et al. 2021a).
Insects can
develop resistance against insecticides through penetration resistance. This
process involves thickening or altering the composition of the cuticle, which
slows down the entry of insecticides into the insect's body. This, in turn,
provides the insect with more time to detoxify the poison. Studies have shown
that this resistance mechanism is caused by changes in the cuticle's structure
and composition (Balabanidou et al.
2018; Chen et al.
2019). Since 1967, there have been reports of penetration resistance in B. germanica (Ku and Bishop 1967), which were followed by other studies (as shown in
Table 1). Some insect pest species that are resistant to insecticides have been
found to have thicker cuticles than susceptible ones (Pedrini et al. 2009; Wood et al. 2010; Lin et al.
2012; Balabanidou et al. 2016; Lilly et al. 2016; Yahuédo et al. 2017; Balabanidou et al. 2019; Verma et al. 2019; Samal and
Kumar 2021; Jacobs et al. 2023).
However, there have been no reports of cuticle thickening in B. germanica.
In Indonesia,
resistant German cockroaches were reported to possess metabolic resistance
mechanisms (Ahmad et al. 2009) and
KDR mutations (Rahayu and Saputra 2022).
However, to our knowledge, there have been no reports regarding penetration
resistance. This study investigated a strain of German cockroach, PLZ-PLM,
origin from Palembang City, the capital of South Sumatra province and one of
the largest metropolitan cities in Indonesia. PLZ-PLM strain has been reported
as propoxur-resistant (Nurseha et al.
2019), and has an LT90 of more than 192 h on six pyrethroid aerosol
insecticides tested (Rahayu et al.
2021a). We conducted further data analysis based on Rahayu et al. (2021a) to determine the resistance ratio of PLZ-PLM strain
to the aerosol insecticides and to detect penetration resistance through the
cuticle thickness of B. germanica,
which is resistant to the pyrethroid-based aerosol insecticides. This
monitoring is intended to provide evaluation data for further insecticide
resistance management, particularly concerning the Palembang population.
Materials and Methods
Sampling and rearing
Two strains were used in this
study, i.e., the PLZ-PLM strain
obtained from Palembang City, Indonesia, and the VCRU-WHO strain (Vector
Control Research Unit-WHO) as the standard strain. Those strains were
maintained in the Animal Physiology Laboratory, Biology Department, Faculty of
Mathematics and Natural Sciences, Universitas Andalas, since 2017 and 2007,
respectively. The German cockroaches used were adult males aged about three
months. The rearing was carried out in plastic containers (30 cm diameter × 27
cm height). The top edge of the container was smeared with a mixture of
petroleum jelly and baby oil and was covered with a thin cloth on the top.
Cockroaches were kept at room temperature between 26–28ºC and a photoperiod of
12:12 (12 h of dark and 12 h of light). They were fed cat food (Pedigree®) and
water ad libitum.
Selection by insecticide efficacy test
The selection was done by
applying six commercial aerosol insecticides with different pyrethroid
formulations (By, Ht, Vp, Fm, Mt, Nm), separately. Ten samples of cockroaches
were placed into a cardboard box (30 cm × 20 cm
× 20 cm), where the top inner edge of the box was layered with paper
tape and smeared with a mixture of petroleum jelly and baby oil to prevent the
cockroaches from escaping. Insecticide was then sprayed from the top of the box
for one second at 1 m from the box base (Fig. 1). Observations were made 24 h
later. The resistant cockroaches were taken from the PLZ-PLM strain that
remained alive, and the susceptible ones were taken from the VCRU-WHO strain.
Five samples were taken for each group.
The left
middle leg was gently detached from the cockroach's body and put on a glass
object. The sample was then dripped with 70% ethanol and cut transversely in
the middle of the tibia using a platinum-coated razor blade. Each leg piece was
then stored in a labeled separate microtube (1.5 mL) containing 70% ethanol
until imaging using SEM.
Preparation and SEM
Samples were immersed in
cacodylate buffer solution for about 2 h, agitated in an ultrasonic cleaner for
5 min, and then soaked in a 2.5% glutaraldehyde solution for 24 h. Next, the
samples were immersed in 2% tannic acid for 6 h, followed by washing with
cacodylate buffer for 5 min, repeated four times. Subsequently, specimens were
dehydrated with graded alcohol starting from 50% alcohol for 5 min, repeated
four times, continuing with 70, 85 and 95% alcohol, each for 20 min at room
temperature. The samples were then immersed in absolute ethanol for 10 min,
repeated twice, and then frozen in tert butanol for 10 min, repeated twice.
Subsequently, samples were frozen in a freezer and dried with a vacuum drier
until dry. After mounting, the specimen was coated with gold metal (Au) and
vacuumed for 15 min. Images were taken using a JSM-5000 LV scanning electron
microscope at the Biological Research Center-Indonesian Institute of Sciences.
Data analysis
The resistance ratio 90 (RR90)
was calculated by referring to data obtained by Rahayu et al. (2021b) with the
formula as follows:
RR90 =
Where RR = resistance ratio,
LT90 = time taken for 90% of a test population to die after insecticide
exposure.
The resistance ratio values were
then grouped into six categories based on Rahayu et al. (2012), namely:
RR90 ≤ 1: absence resistance
1 < RR90 ≤ 5: low resistance
5 < RR90 ≤ 10: moderate resistance
10 < RR90 ≤ 50: high resistance
50 < RR90 ≤ 1000: very high resistance
RR90 > 1000: extremely
high resistance
Table 1: Penetration resistance of B. germanica reported to different insecticides
Study
site |
Insecticide |
Mechanisms |
References |
Virginia,
US |
Carbaryl
(carbamate) |
Slower
penetration |
Ku
and Bishop (1967) |
New
York, US |
Propoxur
(carbamate) |
Reduced
cuticular penetration |
Siegfried
and Scott (1991) |
Florida,
US |
Permethrin
(pyrethroid) |
Reduced
cuticular penetration |
Bull
and Patterson (1993) |
Florida,
US |
Permethrin
(pyrethroid) |
Reduced
cuticular penetration |
Anspaugh et al. (1994) |
Indiana,
US |
Fenvalerate
(pyrethroid) |
Reduced
cuticular penetration |
Wu et al. (1998) |
Florida,
US |
Cypermethrin
(pyrethroid) |
Reduced
cuticular penetration |
Valles
et al. (2000) |
Alabama,
US |
Permethrin,
deltamethrin (pyrethroid) |
Reduced
cuticular penetration |
Wei et al. (2001) |
Alabama,
US |
Permethrin,
deltamethrin (pyrethroid) |
Reduced
cuticular penetration |
Pridgeon
et al. (2002) |
China |
Beta-cypermethrin
(pyrethroid) |
Elevated expression of putative cuticular
protein, and ATP-binding cassette (ABC) transporter |
Zhang
et al. (2014) |
China |
Beta-cypermethrin
(pyrethroid) |
Overexpression
of CYP4G19 (related to biosynthesis
of hydrocarbon) |
Chen
et al. (2019) |
Fig. 1: Diagram of
the selection of B. germanica by
efficacy test, (a) aerosol insecticide, (b) test box area covered with paper
tape and smeared by vaseline + baby oil, (c) test box (d) cockroach samples
Fig. 2: Boxplot of cuticle thickness in B. germanica susceptible and resistant to pyrethroid insecticides.
Dots (°) represent outlier data
Micrographs were
processed using ImageJ v.1.52p. Cuticle thickness was measured by initially
tracing the inner and outer circumference line, whose unclear boundaries due to
debris or damage were not measured (Fig. 2, 3). A total of 25 measurement points
were taken for each sample. The mean cuticle thickness was obtained from the
total cuticle thickness divided by total measurement points. The data collected
were compared by the Mann-Whitney test using SPSS 25.
Results
Table 2: Resistance ratio (RR90) of B. germanica VCRU-WHO and PLZ-PLM strain to six pyrethroid aerosol
insecticides
No |
Insecticide |
Active
ingredient |
Strain |
RR90 (-fold) |
Level
of resistance |
1. |
By |
Cypermethrin
(0.10%) Pralethrin
(0.10%) Transfluthrin
(0.10%) |
VCRU-WHO |
1 |
Absense
resistance |
PLZ-PLM |
18 |
High
resistance |
|||
2. |
Ht |
Transfluthrin
(0.17%) Pralethrin
(0.05%) Cypermethrin
(0.10%) |
VCRU-WHO |
1 |
Absense
resistance |
PLZ-PLM |
42 |
High
resistance |
|||
3. |
Vp |
Dimefluthrin
(0.04%) Pralethrin
(0.12%) Cyfluthrin
(0.03%) |
VCRU-WHO |
1 |
Absense
resistance |
PLZ-PLM |
34 |
High
resistance |
|||
4. |
Fm |
Transfluthrin
(0.15%) Permethrin
(0.15%) |
VCRU-WHO |
1 |
Absense
resistance |
PLZ-PLM |
21 |
High
resistance |
|||
5. |
Mt |
Permethrin
(0.06%) Imiprothrin
(0.03%) Esbiothrin
(0.11%) |
VCRU-WHO |
1 |
Absense
resistance |
PLZ-PLM |
25 |
High resistance |
|||
6. |
Nm |
Transfluthrin
(0.06%) Cyfluthrin
(0.03%) |
VCRU-WHO |
1 |
Absense
resistance |
PLZ-PLM |
45 |
High
resistance |
Table 3: Average cuticle thickness in susceptible and resistant B. germanica to pyrethroid insecticides
Group |
n |
Mean Cuticle thickness (μm) |
SD |
Susceptible |
5 |
8,938 |
1,295 |
Resistant |
5 |
7,887 |
1,337 |
Fig. 3: Micrographs of cross sections of
the left middle midleg of the tibia of Blattella
germanica L. in susceptible (A, B) and resistant (C, D)
individuals with 25 points measuring cuticle thickness (μm)
The RR90 of German cockroach
strains of VCRU-WHO and PLZ-PLM to six aerosol insecticides can be seen in Table
2. The VCRU-WHO strain was susceptible to all tested insecticides. Meanwhile,
the PLZ-PLM strain has an RR90 in the range of 18–45 fold to the aerosol
insecticide used which is classified as highly resistant. The highest and the
lowest RR90 were found in the Nm and By insecticides, respectively.
The
Mann-Whitney test showed an insignificant difference between the cuticle
thickness of the susceptible and the resistant group in the B. germanica (Z = -0.731, P <
0.05; Table 3).
Discussion
Our findings showed the absence
of the cuticle thickening mechanism in the pyrethroid-resistant PLZ-PLM strain.
On the contrary, the susceptible cockroaches (VCRU-WHO) slightly have thicker
cuticles than resistant ones. It seems just the occurrence of individual
variation and is not linked to resistance mechanisms. The absence of cuticle
thickening suggests the presence of other resistance mechanisms in PLZ-PLM
cockroaches, which causes resistant cockroaches to tolerate the insecticide
toxins although not having thicker cuticles, either by increased detoxification
enzymes or mutations in target proteins. However, despite having a thicker
cuticle, the VCRU-WHO strain could not survive insecticide due to the absence
or low level of other mechanisms.
Even though
we cannot accurately determine the resistance level of each mechanism involved,
this study confirmed that the resistance offered by the penetration mechanism
is comparatively lower than other mechanisms. Penetration resistance also
concurrently occurs with other mechanisms that have been proven to contribute
to resistance, as previously reported in B. germanica (Wu et al.
1998) and other species, such as Drosophilla
melanogaster (Strycharz et al. 2013), Aedes aegypti (Kasai et al. 2014) and An. Gambiae (Yahouédo et al. 2017). Nevertheless,
the impact of penetration resistance could strengthen the phenotypic and other
potential resistance mechanisms, allowing insect resistance to expand to
different types of insecticides. Furthermore, this mechanism also allows
insects to tolerate higher insecticide concentrations (Balabanidou et al. 2016), which results in a higher
likelihood of failure in controlling cockroach population. Besides, the absence
of cuticle thickening does not eliminate the possibility of other
cuticle-related resistance mechanisms in PLZ-PLM cockroaches. There may be a
change in the cuticle composition in the resistant cockroaches, which affects
insecticide penetration, such as the finding of Bai et al. (2022), where cuticle melanization is related to the
permeability of the B. germanica
cuticle. Yet, this possibility requires further investigation.
According to
Table 2, the RR90 value showed that PLZ-PLM has high resistance to all tested
pyrethroid aerosol insecticides. Even though the insecticide is a mixture of
several pyrethroid active ingredients, we found differences in the level of
resistance of PLZ-PLM cockroaches to the aerosol insecticides used, where
different compositions produced different insecticidal effects. We also found
that insecticides containing the same active ingredient but in different
concentrations generate distinct insecticidal levels, as observed in the By and
Ht (Table 2). It demonstrates that the efficacy of the insecticide is also
affected by the active ingredient's concentration and composition.
Additional
research is required to investigate other possible factors associated with the
penetration resistance of German cockroaches. Handling the resistance of German
PLZ-PLM cockroaches to commercial aerosol insecticides demands significant
efforts. Developing organic-based bioinsecticides and repellents could be a
potential solution to address the challenge of German cockroach insecticide
resistance. Several previous studies have revealed several bioinsecticides and repellents
that have the potential to control German cockroaches, such as Schinus molle (Ferrero et al. 2007), Cymbopogon flexuosus (Rahayu et
al. 2018), Carica papaya (Rahayu et al. 2020), Morinda citrifolia L. (Rahayu et
al. 2021b), C. nardus (Jannatan
and Rahayu 2021), and organic waste (Jannatan and Rahayu 2023a; Jannatan and
Rahayu 2023b).
Conclusion
The current study confirmed that
the B. germanica PLZ-PLM strain is
highly resistant to six pyrethroid aerosol insecticides (By, Ht, Vp, Fm, Mt,
Nm), but no evidence of cuticle thickening as a resistance mechanism. Further
investigation is needed to determine other resistance mechanisms and the role
of the cuticle in the PLZ-PLM strain to develop effective measures to manage
the resistance of B. germanica.
Acknowledgments
This research was funded by
Universitas Andalas on behalf of Dr. Resti Rahayu, with contract number
T/74/UN16.19/PT.01.03/IS-RPT/2023. Fiscal Year 2023.
Author Contributions
RR designed the study, RR, VHP,
and KWPS performed the experiments, RR and VHP analyzed the data, RR wrote the
paper.
The authors have no conflicts of interest to declare.
Data presented in this study will be available on a fair
request to the corresponding author.
Not applicable.
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