Challenge and opportunity for vector control strategies on key mosquito-borne diseases during the COVID-19 pandemic

Abstract

Mosquito-borne diseases are major global health problems that threaten nearly half of the world’s population. Conflicting resources and infrastructure required by the coronavirus disease 2019 (COVID-19) global pandemic have resulted in the vector control process being more demanding than ever. Although novel vector control paradigms may have been more applicable and efficacious in these challenging settings, there were virtually no reports of novel strategies being developed or implemented during COVID-19 pandemic. Evidence shows that the COVID-19 pandemic has dramatically impacted the implementation of conventional mosquito vector measures. Varying degrees of disruptions in malaria control and insecticide-treated nets (ITNs) and indoor residual spray (IRS) distributions worldwide from 2020 to 2021 were reported. Control measures such as mosquito net distribution and community education were significantly reduced in sub-Saharan countries. The COVID-19 pandemic has provided an opportunity for innovative vector control technologies currently being developed. Releasing sterile or lethal gene-carrying male mosquitoes and novel biopesticides may have advantages that are not matched by traditional vector measures in the current context. Here, we review the effects of COVID-19 pandemic on current vector control measures from 2020 to 2021 and discuss the future direction of vector control, taking into account probable evolving conditions of the COVID-19 pandemic.

Full text

Frontiers in Public Health 01 frontiersin.org
Challenge and opportunity for
vector control strategies on key
mosquito-borne diseases during
the COVID-19 pandemic
Hong-ZhengLu
1,2, 3, YuanSui
4, NeilF.Lobo
5,6, FlorenceFouque
7,
ChenGao
1,3, ShenningLu
1,8, 9,10, 11
, ShanLv
1,8, 9,10, 11 ,12
,
Sheng-QunDeng
2* and Duo-QuanWang
1,8, 9,10, 11 ,12 *
1 Chinese Center for Disease Control and Prevention, National Institute of Parasitic Diseases, Shanghai,
China, 2 Department of Pathogen Biology, the Key Laboratory of Microbiology and Parasitology of Anhui
Province, the Key Laboratory of Zoonoses of High Institutions in Anhui, School of Basic Medical
Sciences, Anhui Medical University, Hefei, China, 3 Department of Epidemiology and Biostatistics, School
of Public Health, Anhui Medical University, Hefei, Anhui, China, 4 Brown School, Washington University,
St. Louis, MO, United States, 5 Malaria Elimination Initiative, Institute for Global Health Sciences,
University of California, San Francisco, San Francisco, CA, United States, 6 Eck Institute for Global Health,
University of Notre Dame, Notre Dame, IN, United States, 7 Research for Implementation Unit, The
Special Programme for Research and Training in Tropical Diseases, World Health Organization, Geneva,
Switzerland, 8 Chinese Center for Tropical Diseases Research, Shanghai, China, 9 WHO Collaborating
Centre for Tropical Diseases, Shanghai, China, 10 National Center for International Research on Tropical
Diseases, Ministry of Science and Technology, Shanghai, China, 11 Key Laboratory of Parasite and Vector
Biology, Ministry of Health, Shanghai, China, 12 School of Global Health, Chinese Center for Tropical
Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China
Mosquito-borne diseases are major global health problems that threaten nearly
half of the world’s population. Conflicting resources and infrastructure required
by the coronavirus disease 2019 (COVID-19) global pandemic have resulted in
the vector control process being more demanding than ever. Although novel
vector control paradigms may have been more applicable and ecacious in
these challenging settings, there were virtually no reports of novel strategies
being developed or implemented during COVID-19 pandemic. Evidence shows
that the COVID-19 pandemic has dramatically impacted the implementation
of conventional mosquito vector measures. Varying degrees of disruptions in
malaria control and insecticide-treated nets (ITNs) and indoor residual spray (IRS)
distributions worldwide from 2020 to 2021 were reported. Control measures
such as mosquito net distribution and community education were significantly
reduced in sub-Saharan countries. The COVID-19 pandemic has provided an
opportunity for innovative vector control technologies currently being developed.
Releasing sterile or lethal gene-carrying male mosquitoes and novel biopesticides
may have advantages that are not matched by traditional vector measures in the
current context. Here, wereview the eects of COVID-19 pandemic on current
vector control measures from 2020 to 2021 and discuss the future direction of
vector control, taking into account probable evolving conditions of the COVID-19
pandemic.
KEYWORDS
COVID-19, mosquito-borne diseases, vector control, mosquito biological control,
mosquito novel control
OPEN ACCESS
EDITED BY
Nuno Sepulveda,
Warsaw University of Technology, Poland
REVIEWED BY
Lara Ferrero Gómez,
Universidade Jean Piaget de Cabo,
CaboVerde
Marta Moreno,
University of London, UnitedKingdom
*CORRESPONDENCE
Duo-Quan Wang
wangdq@nipd.chinacdc.cn
Sheng-Qun Deng
dengshengqun@163.com
RECEIVED 17 April 2023
ACCEPTED 29 June 2023
PUBLISHED 24 July 2023
CITATION
Lu H-Z, Sui Y, Lobo NF, Fouque F, Gao C, Lu S,
Lv S, Deng S-Q and Wang D-Q (2023)
Challenge and opportunity for vector control
strategies on key mosquito-borne diseases
during the COVID-19 pandemic.
Front. Public Health 11:1207293.
doi: 10.3389/fpubh.2023.1207293
COPYRIGHT
© 2023 Lu, Sui, Lobo, Fouque, Gao, Lu, Lv,
Deng and Wang. This is an open-access article
distributed under the terms of the Creative
Commons Attribution License (CC BY). The
use, distribution or reproduction in other
forums is permitted, provided the original
author(s) and the copyright owner(s) are
credited and that the original publication in this
journal is cited, in accordance with accepted
academic practice. No use, distribution or
reproduction is permitted which does not
comply with these terms.
TYPE Review
PUBLISHED 24 July 2023
DOI 10.3389/fpubh.2023.1207293

Lu et al. 10.3389/fpubh.2023.1207293
Frontiers in Public Health 02 frontiersin.org
Introduction
Mosquitoes are the most important vectors for disease transmission
in terms of morbidity and mortality rates. Malaria, dengue fever, and
yellow fever transmitted by mosquitoes have signicantly high
incidences, posing several public health problems (1). More than
600,000 people died of malaria in 2021 (2). Fiy to one hundred million
people were infected with dengue fever annually, which leads to half a
million hospitalizations (3). Infections by or continuous transmission of
yellow fever, chikungunya, and Zika viruses also have signicant public
health impact, threatening more than 40% of the global population (4).
Since the coronavirus disease 2019 (COVID-19) pandemic some
low-income tropical or endemic countries have been unable to sustain
funding for mosquito-borne diseases to ensure control (5).
Investment in the knowledge of the pathogenesis of these mosquito-
borne diseases and antiviral drugs has increased exponentially over the
past 20 years, but progress in the development of eective treatments,
with the exception of malaria, remains slow (6). In the same way, the
development of vaccines against mosquito-borne diseases has never
reached its goals, with the exception of yellow fever. erefore, for many
vector-borne diseases, vector control remains the primary intervention
to control mosquito-borne diseases through several techniques
classied by physical, biological, chemical, genetic, and environmental
aspects. Before the discovery of insecticides in the 1930s and the large-
scale use of insecticides and mosquito nets, vector control interventions
relied primarily on environmental management (7). e focus is on
removing mosquito breeding sites and improving housing by installing
screens to prevent mosquitoes from entering through doors and
windows. is involves the installation of tight-tting screened doors,
screening or closing eaves, and replacing thatched roofs with solid
materials such as metal or tile (8). In the past century, the deployment
of insecticide-treated nets (ITNs), long-lasting insecticidal nets (LLINs),
and indoor residual spraying (IRS) have become the primary and
recommended means of mosquito vector control (7). Signicant
progress in malaria, dengue fever, and Zika viruses, the most important
mosquito-borne diseases, has been achieved through the distribution
of treated mosquito nets to at-risk populations and insecticide spraying.
However, due to the cost issues, and operational constraints, traditional
vector control measures are losing eciency in controlling mosquito-
borne diseases. e benets from these techniques are gradually
plateauing (9). Although multiple strategies are being used and the
development of LLINs and IRS with dierent compounds is
accelerating, the global burden of mosquito-borne diseases on public
health and economies continues to increase (10).
On March 11, 2020, the World Health Organization (WHO)
declared COVID-19 a global pandemic (11). Conrmed cases
emerged in more than 200 countries. Along with the long-standing
challenges of globalization, climate change, urbanization and
insecticide resistance, the mosquito vector control process within the
COVID-19 context was facing unprecedented diculties, further
highlighting the need for new technologies and strategies. A series of
challenges will prevent the critical goals of the WHO Global Strategy
on malaria for 2030 from being met (12). erefore, wemust change
our thinking and adopt innovative and transformative approaches to
vector control. Biological control, represented by the release of sterile
male mosquitoes and new biocides, has excellent potential, but no
reports of novel strategies were developed or implemented during
COVID-19. In this review, we explore the interaction between
COVID-19 and mosquito-borne diseases, and wediscuss promising
vector control strategies within the current environment. Data for this
review were initially identied through a search of PubMed, Web of
Science and ScienceDirect. Weindependently extracted and recorded
data from each eligible study. Specic content and reasons for the
implementation of mosquito vector measures aecting COVID-19
were manually screened to ensure accuracy. Weended up including
19 articles in Table1 that describe the impacts from 2020 to 2021.
Eects of COVID-19 on current
mosquito vector control measures
In the early days of the COVID-19 pandemic, most countries took
measures in the form of lockdowns. In the short term, the lockdown
may have had a positive impact on mosquito-borne diseases by
preventing regional or inter-country transmission of infected
individuals (32). In parallel, the vector will continue to reproduce and
host-seek on humans, alongside a reduction in access to health
facilities and health professionals combined with supply chain issues.
As more countries opened their borders and stopped the lockdown,
the need to reconsider how they balanced COVID-19 with other
epidemics appeared. For example, the complete closure of health and
vector control team activity during the lockdown may have resulted
in increased vector populations (33). Common mosquito-borne
diseases, such as Zika, dengue fever, and malaria, are at risk of
outbreaks (34, 35). Additionally, the co-infection of SARS-CoV-2 and
dengue fever viruses have imposed a signicant burden on healthcare
systems in dengue-endemic regions (36). India imposed its rst
nationwide lockdown on March 24, 2020. Observations were
conducted in two areas of Bangalore, India, comparing data before
and aer the lockdown (February to April 2020, collected once a
month). Compared to February, the Aedes aegypti house index and
Breteau index increased from 6.6 and 9.3 to 26.6 and 34.6, respectively.
Very signicant increase compared to 2017 to 2019 data for this
location (37). In addition to India, mosquito larval site monitoring in
Sri Lanka, Cuba, Indonesia, and Malaysia demonstrated varying
increases (38–41). is suggests that the probability of mosquito-
borne disease outbreaks may increase in places where mosquito
populations become larger. Within this context, mosquito vector
control measures should not bereduced or abandoned but should
begiven more attention. Furthermore, lockdown measures obliged
people to stay much more in their home, where the transmission of
arboviral diseases usually occurs. Cavany etal. (42) used a model to
predict changes in dengue incidence due to lockdown, with the
proportion of people infected in their own homes increasing from
54% in normal conditions to 66% inlockdown conditions, and the
rate of secondary household attacks increasing from 0.109 to 0.128, a
17% increase.
Abbreviations: CI, cytoplasmic incompatibility; COVID-19, coronavirus disease
2019; DENV-2, dengue virus type 2; IIT, incompatible insect technique; IRS, indoor
residual spraying; ITNs, insecticide-treated nets; LLINs, long-lasting insecticidal
nets; RIDL, the release of insects with a dominant lethality gene; SIT, sterile insect
technique; tetO: tetracycline resistance operon; tTA, tetracycline transcriptional
activator; UAVs, unmanned aerial vehicles; WHO, World Health Organization;
ZIKV, Zika virus..

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TABLE1 The eects of COVID-19 on traditional vector control strategies.
Region Location Time Influence Reason Refs
Africa Burundi 2020 to 2021 Severe shortage of health personnel, lack
of conventional vector control products
COVID-19 aects the economic
level leading to inationary
problems
(13)
Congo 2020 LLIN mass distribution campaign
covering approximately 59 million people
in 14 provinces suspended
COVID-19 pandemic outbreak
dominated the political and health
agenda in March 2020
(14)
Comoros 2020 Postponement of ITN and IRS activities Health system overwhelmed (15)
Côte d’Ivoire 2020 Postponement of ITN and IRS activities Health system overwhelmed (16)
Eswatini 2020 COVID-19 pandemic slow and complicate
the planning and preparation of malaria
control programs (e.g., IRS)
e COVID-19 pandemic limits the
movement of people
(17)
Southern Mozambique 2020 COVID-19 pandemic slow and complicate
the planning and preparation of malaria
control programs (e.g., IRS)
e COVID-19 pandemic limits the
movement of people
(17)
Northern Ghana January to April 2020 Closure of malaria clinics, cessation of
routine ITN distribution
Lockdown (18)
Kenya 2021 Median monthly LLIN distribution
declines, mass community distribution
campaign delayed by 10 Months
COVID-19 lockdown strategy and
health workers strike
(13)
Zimbabwe 2020 IRS and ITN distribution suspended,
malaria commodity shortage
Lockdown, curfews, access
restrictions due to the COVID-19
pandemic
(19)
America Brazil 2020 Dengue budget cuts (including the budget
for hospitalization and vector control
measures, such as ITN and IRS)
Health system announced priority
for surveillance and virus
identication of COVID-19
(20, 21)
Coastal Ecuador 2020 Suspension of routine mosquito vector
monitoring and control programs
Coinfection of dengue fever and
SARS-CoV-2 viruses
(22–24)
Honduras 2020 Suspension of routine mosquito vector
monitoring and control programs
Two hurricanes and a sharp increase
in COVID-19 cases
(24, 25)
Asia
Afghanistan 2021 Inecient mosquito net distribution
services and implementation of the
Sehatmandi project were hampered
Internal Conict and COVID-19
pandemic
(26)
Bhutan March to May 2020 Mass distribution of LLIN program
delayed, IRS, health education, and
mosquito vector surveillance disrupted
COVID-19 pandemic caused freight
disruptions, aecting movement of
goods and people
(27)
Meghalaya State, India 2020 National Vector Borne Disease Control
Program conducted in 50 villages, 7 of
which were unable to conduct IRS
activities
Movement restrictions due to
COVID-19
(28)
Pakistan 2020 Water disinfection plan put on hold and
dengue outbreak
Flooding Outbreak and Funds Used
for COVID-19 Prevention Program
(29)
Europe France 2020 Vector control interventions in all overseas
sectors were reduced, social mobilization
campaigns were put on hold, and
preventive insecticide spraying in private
premises was curtailed
Lockdown (30, 31)

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e immediate eect of COVID-19 on mosquito vector control
measures was the massive diversion of medical resources. Budgets for
actions, such as IRS and ITNs, have been massively cut (43). ITN and
IRS dened by WHO as cornerstones of mosquito vector control. e
rapid delivery of ITNs to populations at risk of mosquito-borne
diseases in a remarkably short period of time through mass campaigns
is currently the primary method of ITN operation (44). Governments,
private sectors, and religious and humanitarian organizations have
been working on this for the past few decades, and much has been
accomplished. Sleeping under ITNs has reduced the incidence rate of
malaria by 50% (45). Since the declaration of COVID-19 as a
pandemic, attention has shied to COVID-19, interrupting several
intervention programs for equally health-threatening infectious
diseases (46). Simultaneously, control activities, such as the
distribution of mosquito nets and community education, ceased or
were signicantly reduced (43). e highest levels of mosquito-borne
diseases have been found in sub-Saharan Africa for the past 20 years,
and those regions were then the ones suering most of the
consequences of COVID-19 disruptions. Furthermore, aer the
COVID-19 pandemic, the crowding out of medical resources,
diversion of funds, and interruption of logistics caused by the embargo
made the original control measures impossible to implement (47).
Overall, the impacts of the COVID-19 pandemic during 2020 and
2021 were much larger than envisioned for several mosquito-borne
diseases on dierent continents (Table1).
Varying degrees of disruptions in malaria control and ITNs and
IRS distribution worldwide from 2020 to 2021 were reported (Table1).
According to the WHO, less than half of the 22 million ITNs planned
for global distribution in 2020 had been distributed as of November
2020. Meanwhile, less than half of the routine IRS activities in malaria-
endemic countries have been completed (48). A majority (58%) of
countries (out of 64) report disruptions in the service delivery of their
malaria control programs from 2020 to 2021 (5). Reducing IRS and
ITN allocation is expected to lead to severe consequences. In the most
extreme scenario, conventional malaria control measures, including a
75% reduction in ITN distribution and drug shortages, would increase
sub-Saharan malaria morbidity and mortality rates by more than 20
and 50%, respectively (49). Hogan etal. (50) predicted the extent of
disruption to healthcare and malaria control services during the
COVID-19 pandemic. ey estimated that the global malaria
mortality rate could increase by 36% over the next 5 years, mainly due
to a shortage of ITNs and the scarcity of other essential commodities.
In addition, ITNs and IRS are labor-intensive vector control measures,
the implementation of which inevitably leads to interaction between
communities, in contradiction with the recommendation on
COVID-19 (to avoid crowding). For this reason, the budget for
COVID-19 personal protective equipment in several activities has
been increased (51). Creating more outdoor facilities and improving
indoor air circulation in residential and commercial buildings to
reduce the risk of COVID-19 may increase exposure to
mosquitoes (52).
In addition to the consequences of the COVID-19 pandemic,
several challenges are currently faced by conventional vector control
activities, such as the costs of implementation, traditional mosquito
vector measures, slow operational implementation, and insecticide
resistance (53). e increasing trend of insecticide resistance observed
in recent years is alarming, and resistance to four classes of insecticides
(pyrethroids, organochlorines, carbamates, and organophosphates)
was reported in 32% of the countries with mosquito-borne disease
transmission. e newest approved ingredient in IRS products,
clothianidin, has already been resistant in Central Africa (54).
Moreover, 90% of malaria-endemic countries have reported resistance
to at least one class of insecticides in Anopheles (9). Although ITN-
and IRS-led vector control methods remain valid today against
malaria, their lifespan is shortened. When the COVID-19 outbreak
became a pandemic, new, transformative, and innovative vector
control technologies were already required and are now more strongly
necessary to address the current situation.
Innovative vector control strategies in
development in the current context
Since early 2020, some countries have combined modern
technology with traditional vector interventions to facilitate follow-up.
For example, the ITN distribution was monitored through digital
technology with a mobile application for timely monitoring and
supervisory feedback, allowing more rapid collection of household
statistics and ITN distribution data. is technology allowed for
avoiding contact with personnel to a certain extent (51, 55).
A prior Mexican study used unmanned aerial vehicles (UAVs) to
identify Ae. aegypti breeding sites and spraying to reduce the need for
eld technicians, achieving a 64.9% agreement between UAVs and
ground monitoring. Moreover, UAVs can access breeding sites that
cannot beaccessed or identied by traditional ground monitoring and
disinfection and ensure that routine disinfection and monitoring is
conducted during the lockdown (56). In another case, Gabriel
Carrasco-Escobar etal. used drones in Peru to identify Anopheles
darlingi breeding sites through high-resolution images and
multispectral proles with an overall accuracy of 86.73–96.98% (57).
In addition to collecting mosquito habitats and disinfecting them,
drones are valuable tools for monitoring the environmental factors
that inuence disease dynamics. Flaviviruses are primarily maintained
by wild, non-human primate hosts, and drones can map the migration
patterns of wildlife populations and changes in their habitats. is
brings benets for real-time monitoring of disease dynamics, as well
as vector intervention programs (58, 59).
Releasing sterile or lethal gene-carrying
male mosquitoes
Releasing male mosquitoes as biological insecticides is a cutting-
edge technology with great promise. ese technologies are based on
gram-negative intracytoplasmic bacteria of the genus Wolbachia,
found in 76% of the world’s insect species and is the most widely
distributed commensal bacterium worldwide (60). Manipulation of
Wolbachia strains can induce anti-RNA viral properties in its hosts,
inhibiting the development of pathogens, such as dengue virus and
chikungunya virus, in mosquito vectors (61, 62) and is also associated
with several reproductive operations in mosquito vectors (63). e
result of the CI will bethe suppression of the mosquito population.
erefore, CI-based population control is referred to as an
incompatible insect technique (IIT). Dierent from conventional
mosquito vector control methods, IIT involves the regular release of
Wolbachia-carrying male mosquito populations with appropriate

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Frontiers in Public Health 05 frontiersin.org
methods to reduce the mosquito population size, thus achieving the
goal of disease control. With the study of the principle of CI and the
development of embryo microinjection techniques, progress has also
been made in important mosquito vectors that do not naturally carry
Wolbachia by injecting infected insect cytoplasm or tissue into
mosquito embryos (64). Several successful trials have shown positive
results of Wolbachia in mosquito vector control (65–67).
e sterile insect technique releases large numbers of sterile male
mosquitoes to mate with wild females (68). Sterility methods include
chemical, radiation, hybrid sterility, and chromosomal translocation,
of which radiation sterility is the most commonly used. SIT has the
advantages of being environmentally friendly and controllable on a
large factory scale. For decades, SIT has achieved many successes in
agricultural control and population suppression, and it is currently
widely tested against Culex, Anopheles and Aedes mosquitoes (69–71).
An example, among many others, of an SIT eld trial, was conducted
during the COVID-19 pandemic in southern Germany infested with
Ae. albopictus. Continued release of sterile male mosquitoes from May
to September 2020 was achieved in the trial areas of Ludwigshafen and
Freiburg, with egg sterility reaching 84.7 ± 12.5% and 62.7 ± 25.8%,
respectively; in comparison, the natural sterility in the control area
was 14.6 ± 7.3% (72).
Genetic sterility was also used with the release of insects with a
dominant lethality gene (RIDL). e corresponding gene expression
in the target population is introduced by releasing male transgenic
mosquitoes carrying the dominant lethal gene. e expression of
dominant lethal genes in the currently developed RIDL system is
regulated by the Tet-O system. e lethal gene is under the control
of the tetracycline resistance operon (tetO), a response element of the
tetracycline transcriptional activator (tTA). In the absence of
tetracycline, the tTA activator binds tetO and activates the promoter
to induce the expression of dominant lethal genes. In contrast, in the
presence of tetracycline, tTA binds to tetracycline and prevents it from
binding to the tetO site, thereby inhibiting the system (73). In the wild,
the ospring of RIDL mosquitoes express the gene because of the lack
of tetracycline in their diet, thus achieving control of population
density. Compared to SIT, RIDL does not require manual separation
of males and females, the sex-specic promoter separates males from
females, and there is no reduction in the competitive ability of males
(74). Various RIDL strains have been developed, including A. aegypti,
A. albopictus, and Anopheles gambiae, which are conditionally lethal,
specically lethal, and wingless (73, 75–77).
Extensive trials have demonstrated the feasibility and unique
advantages of releasing sterile or lethal gene-carrying male mosquitoes
for mosquito vector control. In addition to the absence of insecticide
resistance problems associated with traditional methods, long-term
cost-saving benets will address the current funding shortfall due to
COVID-19 (78). In terms of implementation and eectiveness, there
are advantages to using new technologies for mosquito control that
are dicult to match with traditional methods in the current
environment. e biggest challenge for the release of male mosquitoes
carrying sterile or lethal genes is transportation. It is crucial that they
arrive at the release site within 24 h; otherwise, their survival rate,
ight ability, and mating ability can be negatively aected (79).
Unfortunately, the absence of a globally common procedure for the
transport of male mosquitoes makes it challenging to use these new
technologies on a large scale in developing countries. However,
combining multiple control tools and methods, such as geographic
information systems, spatial analysis, or UAV could potentially
improve the current situation and increase sustainability (80, 81).
Other than that, most of these innovative technologies also have
drawbacks that are not yet fully overcome. Larval rearing, eld
monitoring, selection of suitable strains, and construction of models
with optimal solutions for release frequency and time to achieve the
best release strategy have essential eects on control eectiveness (82).
To optimize the utilization of resources and ensure the sustainability
of the control program, new technologies must beintegrated with a
risk stratication system. Incorporating ecient predictive models
and a centralized monitoring approach will signicantly enhance the
practicality of adopting these new technologies (83).
Novel biopesticides
In addition, biopesticides have become popular in recent years
and have certain advantages in the current context. Fungi and bacteria
are the main focus of current biopesticide research. e mechanism
of action between the fungus and host is signicantly complex and
divided into several stages of adhesion, penetration, and colonization.
Fungal spores invade the epidermis and break open the body wall by
forming infestation structures, interfering with the metabolic function
of the host and secreting toxins (84–86). From the perspective of
mosquito control mechanisms, the fungus is highly suitable for on-site
mosquito control. e fungus can attach to mosquito carcasses to
reproduce and create an epidemic within the mosquitoes for
continuous power. Mosquitoes with fungal disease can carry fungal
spores to other mosquito habitats to infect more mosquitoes (87).
Fungal biopesticides have low developmental costs, are convenient to
use, and have considerable eects. ere are no reports on mosquito
resistance to fungal biopesticides (88). ese properties make fungal
insecticides promising for mosquito control. Metarhizium anisopliae
and Beauveria bassiana are more developed than other fungi in fungal
mosquito control. ey can shorten the lifespan of many mosquitoes,
including Anopheles, Aedes, and Culex (89–91). Mosquitoes exposed
to M. anisopliae and B. bassiana die within 3–14 days, and their desire
to suck blood and reproduce is reduced (87, 92). In addition to
aecting survival time and reproductive capacity, M. anisopliae and
B. bassiana have inhibitory eects on mosquito pathogens. Fang found
that recombinant M. anisopliae can prevent the development of
Plasmodium in the vector and can reduce the number of sporozoites
by 98%, indicating that M. anisopliae is eective in ghting against
malaria (93). Deng found that Zika virus (ZIKV) titer levels in the
midgut, head and salivary glands were signicantly reduced aer
feeding ZIKV to Ae. albopictus females (94). Another study found that
Ae. aegypti infected with both M. anisopliae and dengue virus type 2
(DENV-2), and the infection rates of DENV-2 in the heads and
midguts were signicantly reduced (95). As abiotic factors
(temperature, humidity, and ultraviolet radiation) aect the
eectiveness of fungi in eld applications, and the low virulence of the
fungus leads to low eciency of mosquito killing has been an
important reason for its popularity is not widespread. erefore some
researchers have inserted some natural and synthetic genes into the
fungal genome to improve their virulence and tolerance (96). For
example, heat-tolerant genes can be genetically engineered into
M. anisopliae to enhance their adaptability (97). Androctonus australis
insect toxin is a neurotoxin widely used for recombinant expression

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Frontiers in Public Health 06 frontiersin.org
in fungi (98). A prior study reported the toxicity of the recombinant
M. anisopliae formed by this gene in adult Ae. aegypti increased by
nine times (99). In addition, many other genes, such as [SM1]
8
and
scorpine, were recombined into pathogenic fungi to enhance their
control of mosquito-borne infectious diseases (93).
e most mature bacterial biopesticide is Bacillus thuringiensis. It
is a gram-positive, rod-shaped, spore-forming bacterium with
facultative oxygen demand. Its toxin is mainly present in accompanying
spore crystals formed during the development of budding spores (100).
B. thuringiensis is active against Lepidoptera, Coleoptera, Diptera,
Hymenoptera, Homoptera, Orthoptera, and Nematoda, but it is not
toxic to mammals (101, 102). e development of B. thuringiensis var.
israelensis enables B. thuringiensis to beinvested in mosquito control
on a large scale. B. thuringiensis var. israelensis is eective against 72
species of mosquitoes (21 species of Anopheles, 21 species of Aedes, and
17 species of Culex) (103). As a biofriendly insecticide with high
mosquito control eciency, convenient storage, and application forms,
B. thuringiensis has been used in many applications worldwide. e
primary tool for mosquito control in Hawaii, United States, is
B. thuringiensis (104, 105). B. thuringiensis in drinking water is
harmless to humans and well suited for use as a household-level
biocide, and its resistance is dicult to pass on to mosquitoes (106).
ese characteristics make the number of B. thuringiensis unlimited in
the eld of mosquito control, providing a powerful alternative for
mosquito control in the current environment. Another bacterium that
has been relatively successful in mosquito killing is Bacillus sphericus.
B. thuringiensis and B. sphericus have their own advantages and
disadvantages; B. thuringiensis has a broad spectrum of insecticides,
while B. sphericus has a long shelf life (107).
Biological insecticides are more widely used in practical
applications than the release of male mosquitoes for control. ey are
currently used mainly in combination with traditional chemical
insecticides to delay the problem of drug resistance. As an
environmentally friendly tool that is also highly specic and can limit
the growth of target populations in successive generations aer
application, its advantages are clear. It is highly suitable for promotion
in the current environment to address resistance and cost issues (108).
Biological control, represented by the release of male mosquitoes and
biopesticides, can solve many of the pain points of traditional vector
measures in the current context (Table2).
In recent years, natural repellents have gained increasing attention
due to their pure plant ingredients which are low in residue and easy
to degrade. ey are also known for being low or non-toxic, having
minimal skin irritation eects and being environmentally friendly
(116). Natural repellents are primarily derived from various plant
parts such as stems, roots, leaves, owers, and fruits, among others.
e active ingredients of these repellents are mostly esters, ketones,
and alcohols of terpenoids, and they oen contain avonoids and
alkaloids, among others. Currently, the focus on the development of
natural repellents involves the extraction of natural plant products and
the analysis of their active ingredients. is analysis is considered a
hot issue in natural repellent research (117). In addition to the
technologies described above, several mosquito vector control
technologies are still being developed, including acoustic larvicides,
RNAi-based biocides, and nanotechnology, which are equally
desirable. In general, the situation of mosquito-borne diseases during
the COVID-19 pandemic is serious, and the application and
promotion of new vector control strategies should bestrengthened to
eectively reduce the spread of mosquito-borne infectious diseases.
Conclusion
Although the new mosquito vector control technologies
introduced above have signicant advantages over traditional
strategies, the market and practical applications are still dominated by
traditional methods. ere are several reasons for this phenomenon.
(i) e market for new technologies is dicult to guarantee,
resulting in insucient motivation and funding for research
and development, forming a vicious circle.
(ii) Alternative and novel ways of approaching the issue may
combat historical and habitual thinking, allowing new
paradigms to combat the current transmission.
TABLE2 Comparison of traditional vector control (ITNs/LLINs/IRS) and new vector control technologies (the release of male Mosquitoes and
biopesticides).
ITNs/LLINs/IRS The release of male
mosquitoes Biopesticides Refs
Drug resistance Presence Not applicable Complex mechanisms make it
dicult to pass on drug
resistance
(9, 88, 106, 109)
Application method Person-to-person contact Low labor intensity, targeting
mosquitoes, no human contact
Person-to-person contact (52, 78)
Cost e eciency of mosquito control decreases every
year with the increase in drug resistance, and the
cost also increases
saving health personnel, long-
term cost-saving benets
Wide range of sources, cost-
eective, easy to raise and use
(78, 110, 111)
Sustainability Needs to beapplied or replaced regularly Sustainable control can limit the growth of target
populations in successive
generations aer the application
(108, 112, 113)
Environmental impact negative impact Unkn own Environmentally friendly (108, 114)
Eects on the human body negative impact No negative impact High specicity and no negative
impact
(108, 114, 115)

Lu et al. 10.3389/fpubh.2023.1207293
Frontiers in Public Health 07 frontiersin.org
(iii) Previous mosquito vector control focused more on quick
results, especially chemical insecticide-led vector control,
which ignored the long-term benets and environmental and
ecological eects. A scale-down of these control measures
invariably leads to an immediate increase in vectors.
(iv) e standardization process is slow, and larger-scale eld trials
cannot beconducted based on the funding needed.
e COVID-19 pandemic has exposed weaknesses in some
countries’ preparedness and response capacity for public health crises
and the inadequacy of existing mosquito vector control systems. e
COVID-19 pandemic has had a signicant eect on mosquito vector
control and, in its aermath, brings a huge opportunity to improve old
strategies or develop more ecient and resilient ones. At the national
level, epidemics have received unprecedented attention and some tilt
of resources to public health. Systems and structures established as a
result of pandemics may also present new opportunities for mosquito-
borne disease control; for example, the strengthening of community
infrastructure and the system established by the state for monitoring
the spread of COVID-19 also facilitate mosquito-borne disease
projects. Simultaneously, laboratory capacity has improved in many
countries, and the increased power of sequencing technology and
increased level of testing can also beused to strengthen mosquito
vector surveillance activities. At the individual level, more people are
willing to learn about this aspect and pay more attention to epidemic
prevention in their daily lives, which will behelpful for future health
education campaigns on mosquito-borne diseases and the promotion
and implementation of mosquito-borne measures. To alleviate the
current dilemma of mosquito-borne disease in the context of the
COVID-19 and to prevent mosquito-borne disease from becoming
the successive COVID-19, a change in concept, the development of
new technology research, and the accelerated operation of eld trials
are needed.
Author contributions
All authors listed have made a substantial, direct, and intellectual
contribution to the work and approved it for publication.
Funding
is paper was funded by China–Africa cooperation project on
malaria control under the Project (No. 2020-C4-0002-3), the program
of the Chinese Center for Tropical Diseases Research
(no.131031104000160004) as well as UNICEF/UNDP/World Bank/
WHO Special Program for Research and Training in Tropical Diseases
(TDR) Small Grant (WHO Reference 2021/1104003–0) to WDQ, and
National Natural Science Foundation of China (NO. 8210082025) and
Anhui Provincial Natural Science Foundation Project (no.
2108085QH347) to DSQ.
Conflict of interest
e authors declare that the research was conducted in the
absence of any commercial or nancial relationships that could
beconstrued as a potential conict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their aliated organizations,
or those of the publisher, the editors and the reviewers. Any product
that may be evaluated in this article, or claim that may be made by its
manufacturer, is not guaranteed or endorsed by the publisher.
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