Abstract -- The
effectiveness of polymers (paints) enriched with microencapsulated insecticides
against Aedes albopictus was evaluated in laboratory conditions using
the forced contact technique (WHO). Three formulations with different active
ingredients (a.i.) combined with pyriproxyfen (PPF) were evaluated: one contained
a pyrethroid (PY), and two were formulated with organophosphates (OP). The
paints were applied on two types of surfaces and at two concentrations. Nulliparous
adult females without blood ingestion were used to determine the knock-down
effect (KD) in the first 30 minutes, and the mortality rate and time to reach 50%
mortality (TD50) up to 72 hours. Ten bioassays were performed for 27
months after a single initial treatment of the surfaces.
A greater effect was observed when the surface was
more porous and for the higher concentration of PY formulation (KD=25,4% IC 95%
p>0.05 and TD50=16,1% IC 95% p>0.05). Each formulation showed
a different degree of probability for KD and TD50 based on the a.i.
The implications for vector control are discussed
based on studies of different formulations and concentrations of
microencapsulated insecticides in laboratory and field bioassays on different
surfaces.
Keywords -- Aedes albopictus, painting, microencapsulation, Inesfly®.
I. INTRODUCTION
Currently, emerging, and re-emerging vector-borne diseases continue
to be a threat to public health in the context of globalization, urban development,
changing lifestyles, and climate change (WHO, 2017). Therefore, control
strategies based on synanthropic behavior have received increasing attention,
especially with respect to the anthropophilic tendency of Ae. albopictus
(Delatte et al., 2010). Females of this species voluntarily enter the
interior of dwellings to feed on blood and rest, especially if they do not have
abundant vegetation during the day to remain outdoors. Furthermore, in
urbanized areas, Ae. albopictrus colonizes sewage systems, which
provides it with abundant breeding and resting sites that facilitate its
contact with artificial surfaces (Li et al., 2015; Montalvo et al.,
2022).
One system used for the control of these vectors is
the insecticide spraying of residual and thermal fogging (IRS) (Wahid et
al., 2019). Even when the WHO recommended these treatments for indoor and
outdoor applications, IRS could not produce the expected residuality. Moreover,
if mosquito outbreaks persist, the treatments will be repeated at intervals
that coincide with the vector life cycle (WHO, 2009).
Because the IRS enforcement system is highly
restricted in some countries due to its impacts on human health (Gubler and
Clark, 1996), an integrated pest control comprised of simultaneous
methodologies combined with insecticidal paints (IP) could be more effective (Erlanger
et al., 2008).
The use of paints incorporating insecticides (IP)
increases the persistence of pesticides, which extends their period of action
and decreases the number of applications to reduce overall costs in control
campaigns. Conversely to conventional IRS, IP is easy to apply, so specific
training or large-scale logistical planning is required (Schiøler et al.,
2016).
In this study, we evaluated the efficacy of a
paint-like polymer as a new microencapsulation system containing different
insecticides in combination with an insect growth regulator (IGR) at a low
concentration against Ae. albopictus adults. Treated surfaces received
one insecticide treatment at the beginning of bioassays and were evaluated
throughout the test.
According to Inesfly's technology, it is a
microencapsulation process in which the active ingredients (a.i.), such as
conventional insecticides and insect growth regulators (IGR) at low doses, are
introduced into a matrix of polymeric nature formed by chains of vinyl
polymers. This technology allows the gradual release of a.i. in function of the
specific application of the substrate on which the microcapsules are deposited
(Herrero, 2019).
II. METHODS
The study was carried out with a strain of, Aedes (Stegomyia)
albopictus (Skuse, 1894) (Diptera: Culicidae) established and maintained
since 2009 in the Parasitology Laboratory of the Faculty of Veterinary Medicine
of the University of Zaragoza, Spain. For colony maintenance, the usual
breeding protocols are used (Alarcón-Elbal et al., 2010). The mosquito
colony has been used in several investigations and has not been previously
exposed to insecticides.
In the colony, cohorts with approximately 400 adults
were bred in 30×30×30 cm BugDorm-1® retention boxes (Mega View
Science Education Services Co. Ltd., Taichung, Taiwan) with the same age and
equal numbers of males and females. For bioassays, nulliparous females of 3-5
days of age were used and a solution of 10% commercial sugar was offered.
Females were separated using a mouth vacuum and introduced immediately into the
test cones. In each bioassay, 180 females were used.
The efficiency and residuality of formulations were
assessed on different surfaces according to the imbibition power of the
polymer. The three IP formulations with Inesfly technology® contained 5A NG
IGR®= PY formulation (α-cypermethrin 0.7%; d-allethrin 1% + PPF 0.063%), 5A
IGR®= OP formulation (diazinon 1.5%; chlorpyrifos 1.5% + PPF 0.063%) and 5D
IGR®= OP formulation (diazinon 1.5% + PPF 0.063%). The IP formulations were
applied on two surfaces: laminated plasterboard (Pladur®), which is
considered more porous due to its absorption capacity, and pine pinewood slats,
which are considered less porous.
The surfaces were cut into 13×13 cm2 to
ensure the proper fit to the containment cones. Each type of surface was
treated 48 hours before the beginning of the bioassays, following the
manufacturer's recommendations. The paint was manually applied with a regular
brush to each surface at two concentrations. We termed the lower concentration
of 1 kg/6 m2 (recommended) simple primer, which consisted of a
single layer of paint, and termed the higher concentration of 1 kg/3 m2
double primer, which comprised two layers applied 24 h apart.
For each formulation, three replicas were made, and
control treatment consisted of the same type of paint without insecticides or
IGR.
Toxicity bioassays were carried out according to the
standard method of the WHO (1998). For each formulation treatment and control,
groups of 10 females were introduced into the cones using a mouth vacuum and
forced into contact with the surface. A comparative analysis of each
formulation with the control group was carried out based on the potential
mortality after 30 min, discriminating those individuals still affected using
the KD.
An individual was registered as dead if the mosquito
placed on a clean surface was without mobility nor any movement when was
stimulated with a clamp for at least 5 min (WHO, 1994). Individuals, who were
still alive, including those with only ataxia or lack of coordination, were
withdrawn and transferred to hatchers (Mosquito Breeders; Bioquip Products
Inc.) for subsequent mortality monitoring. Once in the hatchers, a 10% sucrose
solution and cotton pieces moistened with dechlorinated water were placed on
top of the grids of the air inlet hatcher. Immediately, we began counting the
number of dead individuals for each replica, including its control, from 30 to
60 min after forced contact (KD), observing the accumulated mortality at 60
min, 24 h, 48 h, and 72 h. The mosquitoes that were dying remained inside the
hatchers since there was a risk of causing death by the constant manipulation
of individuals still alive. Ten individual bioassays were performed with a
single initial treatment of the surfaces and distributed at three-month
intervals. The entire experiment lasted 27 months
Statistical analysis: Due to the low
variability between replicates, the results obtained for the three replicates
of each bioassay were combined. The mortality rate each was corrected based on
the mortality of control using Abbott's (Abbott, 1987) formula.
To assess the potential effect of surface,
formulation, concentration, and time, on the KD effect and the mortality
observed at different intervals post-exposure, we created a surrogate variable
of mortality for this period which consisted of the time estimation (in hours)
in that caused the death of 50% (TD50) of the specimens in each
bioassay. For each interval (30 to 60 minutes, 24, 48, and 72 hours), the
estimated time of death was calculated as the midpoint between that observation
interval and the immediately preceding one.
For KD analysis, a multivariate logistic regression
model (MLGz) was adjusted. The dependent variable of dichotomous nature was an
indicator of whether the individual exhibited a KD effect at 30 minutes after
exposure, using a logit link function (multivariate logistic regression). All
experimental variables (surface, formula, applied concentration, and time) and
their second-degree interactions were introduced as predictor variables in the
initial model. All variables were categorical, except the time, which was a
continuous variable representing the months elapsed since the first bioassay
was performed.
For analysis of the TD50, a
general multivariate linear model (GLM) was adjusted, with the TD50
as a dependent variable and the same predictors considered in the KD analysis,
including their second-degree interactions.
Both models were adjusted considering the less porous
surface (pinewood), the double concentration, and the 5D IGR® formulation
as base levels of the categorical variables. To refine the initial statistical
models and obtain a better fit in the final models, a better model selection
algorithm based on the Akaike information criterion (AIC) was used (Akaike,
1973; Anderson et al., 2000).
III. RESULTS
Flip effect:
The IP formulations of 5A NG IGR® and 5A IGR® showed a significantly
high KD effect of 100% up to 12 months. Subsequently, these formulations
presented values of 90% of females affected. Both concentrations of 5D IGR®
formulations exhibited the lowest KD effect, which was never higher than 70%
and progressively decreased reaching 30-40% in the last bioassay.
The final model adjusted to the entire KD data
preserved eight parameters that explained 77% of the deviation (Table 1).
According to the final model obtained, main effects showed that, in general,
the KD magnitude was higher on the most porous surface (plaster) and lower at
the recommended concentration. Additionally, KD probability was highest for 5A
NG IGR®, medium for 5A IGR® and lowest for 5D IGR®.
Figure 3. Least squares values (95% CI) estimated by
the final regression model for the median probability of death to 50% death (TD50).
A=
TD50 according to the type of surfaces and the dose applied:
1 kg/6 m2 (recommended); 1 kg/3 m2 (double). B=
TD50 according to the type of surface, more porous (plaster)
or less porous (pinewood), and formulations applied.
5A NG IGR®= α-cypermethrin 0.7%, d-allethrin
1%, PPF 0.063%; 5A IGR®= diazinon 1.5%, chlorpyrifos 1.5%, PPF 0.063%; 5D IGR®= diazinon 1.5%, PPF
0.063%.
for the
less porous surface was significantly lower but it was noticeably much more
effective at the beginning of the test. The effect between the type of formulation
and the time (month) also showed differences between formulations containing PY
vs. OP, i.e., the TD50 of the three formulations at the start
of the test was similar, but 5A NG IGR® (PY) maintained its efficacy
throughout the test and the effect that was further increased at the high concentration.
IV. DISCUSSION
The IRS insect vector control strategy is widely used. However, IRS
is partially used because mosquitoes tend to rest inside dwellings after
feeding, leading to increased synanthropic interactions (Fullman et al.,
2013). In this regard, it has been reported the microencapsulation methodology
that includes the use of IP shows better results since its effectiveness was demonstrated
on different surfaces (Mashauri et al., 2017; Acharya et al.,
2021; Ngwej et al., 2021). The active ingredients are gradually released
according to the treated area, the type of surface, the concentration applied,
and the residual effect.
Studies performed with the same IP microencapsulation
technology (Inesfly®) in field and laboratory conditions have proven
its effectiveness. Although these studies did not all use the same a.i. as in
this study, we cite some: Anopheles gambiae; Culex quinquefasciatus
(Mosqueira et al., 2010a, 2010b, 2015); Rhodnius prolixus (Oliveira
Filho, 1997); Triatoma infestans (Gemio Alarico et al.,2010;
Gorla et al., 2015; Dias and Jemmio, 2008; Maloney et al., 2013;
Amelotti et al., 2009; Banjara et al., 2019); and Estegomya
albopicta= Aedes albopictus (Yao et al.,2015; Junnila et
al., 2015).
Mosqueira et al. (2010a) compared the
effectiveness of the IP formulation (5A IGRMT) in the
laboratory against mosquitoes of the genus Culex. The formulations applied were
composed of two OPs, chlorpyrifos (1.5%), diazinon (1.5%), and pyriproxyfen (0.063%)
to the two types of surfaces, demonstrating high mortality (87–100%) up to six
months on less porous surfaces. Furthermore, one-year post-treatment recorded
high mortality rates (93-100%) on less porous surfaces (pinewood) for both
concentrations. However, the high effectiveness of a.i. on porous surfaces
disappeared six months after treatment against resistant and susceptible
mosquitoes. Compared with our results, although the TD50 at the onset
of the experiments was similar for both PY and OPs, PY (5A NG IGR®)
was not affected by the degradation of a.i. and maintained their residual
effectiveness throughout the trial. However, the degradation of the a.i. in the
OPs (5A IGR® and 5D IGR®) decreased their
effectiveness by 52% for both at 27 months, so it could be assumed that the
type of surface affects the efficiency, especially for the most porous types,
since surfaces with a less dense porosity (plaster) were used in this study
compared with those used by Mosqueira et al. (2010a). However, the nature
of the surface may be one of the most important factors in the effectiveness of
any PI (Correa et al., 2019).
Previous research (Jenson et al., 2009) observed that the
surface to which PIs are applied, especially more porous surfaces, generally results
in lower effectiveness compared to a less porous one, though the environmental
conditions to which it is exposed may influence its residual effectiveness
(Bennett et al., 2010).
Another factor may be the concentration applied to
each surface, as two-layer treatment results in a longer duration of efficacy. Gunasekaran
et al. (2005) described the difficulty of achieving good surface coverage
to estimate the reduction of the IRD. Therefore, increased coverage of treatment
may lead to an increase in the duration of IRD suppression. Other authors, such
as Ratti et al. (2018), suggested that additional spraying or the use of
two layers (double concentration) on 50% of the surfaces to be treated was
effective in reducing the IRD and as effective as using a single layer on 70%
of the surface.
When analyzing the mortality data, it was necessary to
quantify the survival of the exposed individuals, as the type of surface,
formulation, and concentration affect the TD50, which was
be maintained or increased in each bioassay as time passed.
Although both surfaces produced similar mortality
rates, the TD50 on the less porous surface increased significantly when
the concentration was doubled, i.e., the TD50 on the less porous
surface was 1.7 times faster than for the most porous surface at high
concentration with an approximate difference of 9.2 hours. To produce the TD50
in a shorter time, the surface conditions were 37.5% more effective if the
concentration was doubled. The most important issue demonstrating the high
residuality of the PI is the degradation or volatilization of the insecticides
applied in these surfaces (Arthur et al., 2009), in addition to factors
that could condition their efficacy and residuality, such as the concentration,
formulation of the a.i. and especially the type of surface.
The variables analyzed did not allow to elucidate
whether the mortality after KD was produced by its interaction with the i.a. or
by underlying mechanisms, since not necessarily the lethal action could be
associated with the type of i.a. (Alzogaray et al., 1997). This
contrasted with mortality, which could have occurred after survival to KD (Briggs
et al., 1976) and may have depended on factors such as the insecticidal
interaction of each formula, the faster penetration of a.i. to the mosquito,
the concentration or availability of release of microcapsules with respect to
the type of surface and metabolic degradation. However, the persistence of the
above-mentioned effects related to subsequent mortality was constant and
effective at the start of bioassays, especially in PY (5A NG IGR®) and OP
diazinon + chlorpyrifos (5A IGR®). On the contrary, the formulation
with a single i.a. OP (5D IGR®) presented a lower lethality, which
was gradually decreasing, evidencing that the surface in relation to the i.a.
influenced its effectiveness. We must clarify that, the determination of the
probability of KD was reduced as the a.i. of the three formulations degraded
over time, especially for OPs. This suggests that, in determining the
correlation between the rate of KD and TD50 for each treatment, it
is possible that all individuals with the KD effect could have presented a
false diagnosis of death, regardless of the lethal effect of each i.a.
Similar studies by Ajayi et al. (2020) observed
a KD rate of 100% for mosquitoes within 10 min after exposure in the first two
months, and a lengthening of the time of the KD due to degradation of the
active ingredients. Unlike our results, the combined OPs diazinon and
chlorpyrifos (5A IGR®) recorded high KD effects (90%)
even up to 24 months, although variations in their efficacy were evident,
especially for the less porous surface. These differences were maintained even
a high concentrations. Therefore, when the surface is more porous, the KD
increases, which may imply that the properties and porosity of the surface
facilitate the exit of microcapsules (Williams et al., 1982).
The basis of comprehensive control strategies must be
decisive, especially in developing countries, as communication and assessments
of changes in social behavior on vector-borne diseases are steadily increasing,
and new methodologies for the control and management of IRS programs are gaining
acceptance (Kebede et al., 2020). The use of methodologies for the
microencapsulation of insecticides that are more sustainable for the
environment or the use of nanoparticles containing insecticides could be investigated
(Norris et al., 2020), whether chemically or biologically based.
V. CONCLUSIONS
Compared to other mosquito species (Mosqueira et al., 2010a;
2010b), in our study, the IP analyzed under laboratory conditions could have
significant efficacy on one of the species of the genus Aedes, and its
application on similar surfaces or concentrations and their interactions
confirm their interest in the control of this species. Therefore, even after 27
months of a single initial application, the results showed high mortality
(100%). Reaffirming the effectiveness and residuality of PY (5A NG IRG®)
vs. OP (5A IGR® and 5D IGR®) allows for us to
reach the following conclusions:
The results show that the efficacy of PY-based
formulations is not conditioned by the type of surface or concentration and they
maintain residuality up to 27 months after a single treatment.
For the residuality, the coefficient of the model
indicates that the number of hours elapsed from the first 30 minutes to the
death of 50% of the specimens (TD50) was greater for a more porous
surface. This conditioning was affirmed by the type of surface and the
contraction, but not by the type of microencapsulated a.i. However, the high concentration
did not affect the TD50 of the more porous surface but the TD50
is reduced on the less porous surface. That is, in the latter case, mortality
occurred in a shorter time, although this result may be conditioned by the type
of active ingredient.
Conversely, if the surface is less porous, its
effectiveness may be greater initially, although the higher mortality in the
lowest number of hours in our study was recorded with PY (5A NG IGR®)
on a more porous surface. If a surface is more porous, TD50 mortality
occurs more effectively in a shorter time in the presence of PY or with OP. However,
on a more porous surface and at a recommended concentration, the mortality
values were significantly lower than on a double-primed surface.
Because the chemical composition of insecticides in
microcapsules may contribute to a variation in bioavailability on less porous
surfaces, no differences were observed in the mortality estimates, and the TD50
was similar for all three formulations.
Long-term assessments on Aedes mosquito populations in
field conditions should be performed to complement control programs in areas of
high epidemiological risk, such as Latin America or Africa, and include other
vector species (leishmaniasis).
According to our results, IP could become an effective
additional tool for the control of Ae. albopictus, as formulations with mixtures
of insecticidal ingredients with greater residual powder provide greater
efficacy.
Acknowledgment
This study was funded by SGI Project Number 218304 of the Department
of Science, Technology and University of the Diputación General de Aragón and
the Social and Cultural Work of Ibercaja.
It was partially supported by the Research Group Funds of the Government
of Aragon (A05-17R).
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Received: August 16, 2021
Sent to Subject Editor: September 16, 2021
Accepted: April 23, 2022
Recommended by Subject Editor Maria Laura Foresti
