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Systematic Review
Revised

Current status of insecticide resistance in malaria vectors in the Asian countries: a systematic review

[version 2; peer review: 1 approved, 2 approved with reservations]
PUBLISHED 04 Jan 2022
Author details Author details
OPEN PEER REVIEW
REVIEWER STATUS

Abstract

Background: The application of insecticides for malaria vector control has led to a global problem, which is the current trend of increased resistance against these chemicals. This study aimed to review the insecticide resistance status was previously determined in Asia and how to implement the necessary interventions. Moreover, the implications of resistance in malaria vector control in this region were studied.
Methods: This systematic review was conducted using a predefined protocol based on PRISMA-retrieved articles from four science databases, namely ProQuest, Science Direct, EBSCO, and PubMed in the last ten years (2009 to 2019). The searching process utilized four main combinations of the following keywords: malaria, vector control, insecticide, and Asia. In ProQuest, malaria control, as well as an insecticide, were used as keywords. The following criteria were included in the filter, namely full text, the source of each article, scholarly journal, Asia, and publication date as in the last ten years.
Results: There were 1408 articles retrieved during the initial search (ProQuest=722, Science Direct=267, EBSCO=50, PubMed=285, and Scopus=84). During the screening, 27 articles were excluded because of duplication, 1361 based on title and abstract incompatibility with the inclusion criteria, and 20 due to content differences. In the final screening process, 15 articles were chosen to be analyzed. From the 15 articles, it is known that there was organochlorine (DDT), organophosphate (malathion), and pyrethroids resistance in several Anopheles species with a less than 80% mortality rate.
Conclusion: This review found multiple resistance in several Anopheles includes resistance to pyrethroid. The reports of pyrethroid resistance were quite challenging because it is considered effective in the malaria vector control. Several countries in Asia are implementing an insecticide resistance management (IRM) strategy against malaria vectors following the Global Plan for IRM.

Keywords

Anopheles; Malaria Elimination; Vector Control Program; Insecticide Resistance; Asian Countries

Revised Amendments from Version 1

This manuscript is a revision version. The revision was based on reviewers' comments and suggestions. It is shown from abstract to conclusion, and also, there are several additional references to conform all the words. The important thing is the conclusion; this is drawn from the article selected. There are new titles given; the results and discussion improved; all revisions are based on the reviewers' comments and suggestions. We hope this paper will be more readable and understandable for others.

To read any peer review reports and author responses for this article, follow the "read" links in the Open Peer Review table.

Introduction

Malaria is one of the most common vector-borne diseases widespread in the tropics and subtropics1. According to the World Malaria Report (2020), an estimated that around 229 million cases of malaria in 2019 in 87 Malaria endemic countries, declined from 238 million in 2000 in 108 countries which were malaria endemic in 2000. Malaria death has been reduced in the period 2000–2019, from 736,000 in the year 2000 to 409,000 in 20192. The global estimate of deaths caused by malaria reached 435,000 cases, which was the same number in 20163. The use of insecticides is the basis for the effective control of vectors, and this process has played an essential role in the management and elimination of malaria4.

The prevention of malaria depends on four classes of insecticides mailny one class of insecticides, namely pyrethroids; however, the increase in resistance to it reduces this treatment's efficacy and it is dangerous5. The progressive reduction of malaria's burden through substantial improvements of insecticide-based vector control in recent years is partly reversible by the emergence of widespread resistance to this chemical6. Insecticide resistance is widespread and is now reported in almost two-thirds of the countries with ongoing malaria transmission. This resistance affects all major vector species and groups of insecticides7.

Vector control is an essential aspect of a program organized to manage the disease transmitted by Anopheles mosquitoes. The use of insecticides for this process is an effective strategy; however, it is also related to the development of resistance in targeted vectors and is one reason for the failure of disease control in many countries8. Since 2000, malaria cases have halved due to the management and vector control interventions, estimated to have saved 660 million people9. The global commitment to eliminate malaria by 2030 requires immediate efforts that include the establishment of infrastructure for regular monitoring insecticide resistance, the development of combined and effective control products10.

This review aimed to determine the status of insecticide resistance in Asia and how to implement interventions. It is also expected that this sets an example for other countries in the vector control program and provides guidance for insecticides and malaria risk reduction.

Methods

Search strategy

This study retrieved articles from four science databases, namely ProQuest, Science Direct, EBSCO, and PubMed, from December 2009 to December 2019. A systematic review was conducted using a predefined protocol based on the preferred reporting items for systematic reviews and meta-analyses (PRISMA)11,12. The searching process utilized four main combinations of the following keywords: “malaria”, “vector control”, “insecticide”, and “Asia”. In order to reduce the risk of bias from the articles obtained, the researchers conducted disbursements in all databases using the same keywords and on the same day.

In ProQuest, “malaria” and “vector control”, as well as “insecticide”, were used as keywords. The full text, the source of an article, scholarly journal, Asia, and date of publication as in the last ten years were included in the filter. The search strategy and filter used in Science Direct were the same as that above except "Asia". In EBSCO, a similar keyword was also used. The limiters were the same as the filter in the ProQuest, but also included "abstract available". In the PubMed, the terms used were as follows, ("malaria"[MeSH Terms] OR "malaria"[All Fields]) AND ("vector"[MeSH Terms] OR "vector"[All Fields]) AND ("control"[MeSH Terms] OR "control"[All Fields]) AND ("insecticide"[MeSH Terms] OR "insecticide"[All Fields]) AND ("loattrfulltext"[sb] AND "2009/12/02"[PDat] : "2019/12/02"[Pdat])s.

Inclusion and exclusion criteria

Original articles (academic or research papers) in Asia, written in English and published in the last ten years were included. Study designs such as prospective study, review, cross-sectional, cohort, and case-control were included. Articles about biochemical, resistance to dieldrin (RDL) mutation, knowledge and attitudes, and spatial modeling were excluded because that can cause different results. Articles about malaria but including nothing about insecticides were excluded. The implications of insecticide resistance in related countries were investigated. Studies that were not relevant to this study were excluded.

Study selection

The articles' eligibility was determined from each title, abstract, and full text by two reviewers (DP and DS). DP and DS also independently screened the articles for inclusion and extracted data on general information. To solve any disagreements and problems during the study, regular meetings were held by the researchers to discuss issues.

Data extraction and analysis

The search strategy and inclusion and exclusion criteria were validated and implemented. The initial database was then created from the electronic search. All citations were first filtered by title and abstract, and duplicates omitted. The full texts of eligible papers were then obtained independently for further filtering. After resolving the differences in data extraction or interpretation through consensual discussions based on the inclusion and exclusion criteria mentioned above, the final papers were selected.

The data from the chosen eligible studies were the authors, study period, year of publication, the country where it was conducted, study period, publisher, settings, location characteristics, bioassay methods, the sample of Anopheles mosquito, and habitat. The findings were arranged according to the objective and results obtained in related implications of malaria vector control resistance. Throughout the entire selection process, the use of insecticides in the bioassay method, the associated mortality rate of the Anopheles mosquito, and its implementation in the specific areas were reported to illustrate the practice's pattern and extent.

All variables for which we extracted data ware Anopheles species, vector habitat, bioassay method, insecticides, mortality rate, insecticide resistance strategies/intervention. The differences in methods could bias the results; to reduce this bias, we selected articles with a similar method. For articles about insecticide resistance, we only looked at articles using bioassay with the world health organization (WHO) standard13. Even though currently the CDC bottle assay is also used for insecticide resistance testing and monitoring, there was no selected articles used CDC bottle assay for testing insecticide resistance and monitoring. The WHO bioassay is carried out with paper impregnated from four main classes of insecticides in common use, with different concentrations according to the WHO test procedure14.

Results

A map showing the countries where insecticide resistance has been reported and the recorded resistance status for each insecticide used is missing shown in Figure 115. There were 1,408 articles retrieved during the initial searching (ProQuest=722, Science Direct=267, EBSCO=50, PubMed=285 and Scopus=84). Through screening, 27 articles were excluded because of duplication, 1,361 based on title and abstract incompatibility and 20 due to inconsistency with the inclusion criteria; 15 were chosen to be analyzed.

c2345dba-5905-449f-bbd0-e1fd0a94eeb9_figure1.gif

Figure 1. PRISMA flow diagram of systematic review inclusion and exclusion process.

The 15 eligible articles originated from eight Asian countries published from 2012 to 2019 journals are shown in Table 1.

Table 1. Article describtion.

AuthorsTitleYear of piblicationCountryStudy periodsPublisherReference
Ahmad et al.Status of insecticide resistance in high-risk malaria
provinces in Afghanistan.
2016AfghanistanAugust to October 2014Malaria Journal20
Mishra et al.Insecticide resistance status of Anopheles culicifacies in
Madhya Pradesh, central India
2012IndiaAugust to September 2009Journal of Vector-
Borne Diseases
8
Dhiman et al.Insecticide resistance and human blood meal preference
for Anopheles annularis in Asom-Meghalaya border area,
northeast India
2014IndiaJune–August 2011Journal of Vector-
Borne Diseases
21
Sahu et al.Triple insecticide resistance of Anopheles culicifacies: A
practical impediment for malaria control in Odisha State,
India.
2015IndiaApril to June 2014Indian Journal of
Medical Research
19
Chand et al.Insecticide resistance status of An. culicifacies in Gadchiroli
(Maharashtra) India
2017IndiaAugust 2016 and February
2017
Pathogens and
global health
22
Chareonviriyaphap
et al.
Review of insecticide resistance and behavioral avoidance
of human diseases by vectors in Thailand
2013Thailand2000–2010Parasites & Vectors 23
Chaumeau et al.Insecticide resistance of malaria vectors along the
Thailand-Myanmar border
2017ThailandAugust and November 2014,
July 2015
Parasites & Vectors 24
Sumarnrote et al.Insecticide resistance status of Anopheles mosquitoes in
Ubon Ratchathani province, Northeastern Thailand
2017Thailand September 2013–September
2015
Malaria Journal 17
Gorouhi et al.Biochemical Basis of Cyfluthrin and DDT Resistance in
Anopheles stephensi (Diptera: Culicidae) in Malarious Area
of Iran
2018IranApril–June 2015Journal of
Arthropod-Borne
Diseases
25
Vatandoost et al.Indication of pyrethroid resistance in the main malaria
vector, Anopheles stephensi from Iran
2012IranSpring 2011Asian Pacific Journal
of Tropical Medicine
26
Marcombe et al.Insecticide resistance status of malaria vectors in Lao PDR2017LaoThe rainy (June to October)
and dry (January to May)
seasons of 2014 and 2015
PloS One 27
Qin et al.Insecticide resistance of Anopheles sinensis and An. vagus
in Hainan Island, a malaria-endemic area in China
2014ChinaJuly–August 2012Parasites & Vectors 28
Dai et al.Development of insecticide resistance of malaria vector
Anopheles sinensis in Shandong Province In China
2015China2003–2012Malaria Journal 29
Surendran et al.Variations in susceptibility to common insecticides and
resistance mechanisms among morphologically identified
species of the malaria vector Anopheles subpictus in Sri
Lanka
2012Sri Lanka July 2008–June 2010 Parasites & Vectors 30
S.İ. Yavaşoglu,
et al.
Current insecticide resistance status of Anopheles sacharovi
and A. superpictus in former malaria-endemic areas of
Turkey
2019TurkeyApril 2014 and September 2015ActaTropica 31

There were 23 species of Anopheles from these studies (Table 2). The main vectors included An. stephensi (Iran), An. superpictus (Afghanistan), An. culicifacies (India), An. minimus and An. maculatus (Lao and Thailand), An. sinensis (China), An. subpictus (Sri Lanka), and An. sacharovi (Turkey). From Table 2, the habitat of malaria vector was divided into four habitats: 1) Agriculture: rice fields (paddy fields), 2). Mountains (forest), 3). Aquatic habitat (rivers, ponds, streams, swamps), and 4) Coastal (seaport). In India, An. cullicifatus was found only in the forest, but An. annularis was found in the forest an irrigation pond. Anopheles cullicifatus in Afghanistan was found together with An. stephensi and An. superpictus at agriculture and aquatics habitat. Anopheles annularis was also found in Thailand on Agriculture (paddy fields). In Iran, there was only An. stephensi was found in coastal areas and ports. In coastal and inland Sri Lanka was discovered An. subpictus and An. sundaicus. In Thailand and Lao, many species were found in forests and agriculture (paddy fields) such as An. annularis, An. minimal, An. hyrcanus, An. barbirostris, An. vagus, An. maculatatatus, An. jamessi, An. scanloni, An. kochi, An. tesselatus, An. dirus, An. karwari, An. nivpes, An. vagus, An. philipinensis. As same as in Thailand, in Lao there were also many species of Anopheles in the same habitat, except An. umbrosus and An. aconitus were in Lao and An. jamessi, An. scanloni in Thailand. In China, there were two species in mountains, aquatics habitat, and agriculture; they were An. sinensis and An. vagus. Anopheles superpictus, besides being found in Afghanistan, also in Turkey together with An. sacharowi on the farm, waters, and swamps. The differences in the main vector of each country depended on environmental/ecological conditions, living habitat, as well as the feeding and resting behavior of each Anopheles.

Table 2. Mosquito species and their types of habitat.

Study locationCountryAnopheles
species
Sample
adult female
mosquitos
(n)
Vector habitatReference
Nangarhar, Laghman, Kunar, Ghazni, and
Badakhshan
AfghanistanAn. stephensi,
An. superpictus,
An. culicifacies
2049Ricefield, river
stream, ponds, and
water puddle
20
Madhya Pradesh IndiaAn. culicifaciesNAForest8
Asom-Meghalaya border area, northeast India IndiaAn. annularis200Forest, ponds
irrigation
21
Rayagada, Nowrangpur, Kalahandi, Malkangiri
and Koraput
IndiaAn. culicifacies1740Forest19
Gadchiroli district IndiaAn. culicifaciesNAForest 22
Chiang Mai-Chiang Dao, Mae Hongsom, Phrae ThailandAn. minimus
An. annularis
NAPaddy fields and
rivulet
23
Thailand-Myanmar Border ThailandAn. annularis,
An. minimus,
An. hyrcanus,
An. barbirostris,
An. vagus,
An. maculatus,
An. jamessi,
An. scanloni,
An. kochi,
An. tesselatus
5896Agriculture24
Khong Chiam, Sirindhorn, Buntharik, and
Nachaluay
ThailandAn. hyrcanus,
An. barbirostris,
An. maculatus,
An. nivipes,
An. philipinensis,
An. vagus
An. dirus
An. karwari
2088Forest and ricefield17
Chabahar Seaport, southeast corner of Iran IranAn. stephensi317Seaport25
Sistan and BaluchistanIranAn.stephensi733Coastal 26
Phongsaly, Bokeo, LuangPrabang, Vientiane
Pro, Borlikhamxay, Khammouane, Savannakhet,
Saravane, Sekong, Attapeu.
LaoAn. minimus,
An. hyrcanus,
An. vagus
An. maculatus
An. nivipes
An. philipinesnis
An. umbrosus
An. kochi
An. tesselatus
An. aconitus
3977Forest, village,
agriculture
27
Hainan Island ChinaAn. sinensis,
An. vagus
1468Mountainous and
ricefield
28
Shandong ProvinceChina An. sinensis4370Irrigated ricefield,
aquatic habitat, and
small ponds
29
Batticaloa, Puttalam, Trincomalee and Ampara Sri LankaAn. subpictus
An. sundaicus
256Coastal and inland30
Southeastern Anatolia and the Mediterranean TurkeyAn. superpictus,
An. sacharovi
1230Agricultural, ponds,
stream and swamps
31

All the female Anopheles collected were morphologically identified for their species/complexes using stereomicroscopes and morphological keys16. The mosquitoes were separated by species/complexes for bioassays. The mosquitoes kept alive by giving them a sugar solution17.

Anopheles mosquitoes were morphologically identified at the adult stage using the Glick identification key18. The susceptibility tests were carried out following the WHO guidelines for monitoring resistance in malaria vectors. From 15 papers reviewed, the papers impregnated with insecticides of DDT (4%), malathion (5%), bendiocarb (0.1%), propoxur (0,1%), deltamethrin (0.05%) and l-cyhalothrin (0.05%), cyfluthrin 0.15%, permethrin 0.75%, and etofenprox 0.5% were prepared by adopting the WHO standard method14 (Table 3).

Table 3. The WHO bioassay method.

CountryWHO bioassay with insecticides
OrganochlorineOrganophosphateCarbamatePyrethroid
DDT (%)malathion (%)Bendiocarb
(%)
Propoxur
(%)
Permethrin
(%)
Deltamethrin
(%)
Lambda-
cyhalothrin (%)
Cyfluthrin
(%)
Etofenprox
(%)
Afghanistan4.05.00.1NA0.750.05NANANA
India4.05.0NANANA0.05NANANA
India4.0NANANANA0.05NANANA
India4.05.0NANANA0.05NANANA
India4.0NANANA0.750.050.050.15NA
Thailand4.0NANANANANANANANA
Thailand4.0NANANA0.750.05NANANA
Thailand4.0NANANA0.750.05NANANA
Iran4.0NANANA0.750.050.050.150.5
Iran4.0NANANA0.750.050.050.150.5
Lao4.0NANANA0.750.05NANANA
China4.05.0NANANA0.05NANANA
China4.05.0NANANA0.05NA0.15NA
Sri Lanka4.05.0NANANA0.050.05NANA
Turkey4.05.0NA0,10,750,05NANA0.5

WHO=world health organization. DDT=dichlorodiphenyltrichloroethane. NA= not available.

The insecticide bioassay was then carried out using a recommended standard WHO kit13. The mortality rate was recorded 24 hours after exposure, while the average death was calculated for each insecticide and according to the WHO criteria19. Bioassy results according to the WHO citeria are susceptible (≥98% mortality), possible resistance (90–97% mortality) or confirmed resistance (<90% mortality13.

The highest mortality rate (MR) ≥ 98% of etofenprox application was on An. stephensi in Iran. While permethrin application was on An. superpictus (Afghanistan), An. nivipes (Thailand), An. philipinensis (Lao and Thailand), and An. tesselatus (Lao). Then, bendiocarb and malathion were on An. culicifacies (India and Afghanistan). Also, deltamethrin was on An. anularis (India), An. barbirostris, An. dirus, An. karwari (Thailand), An. vagus (Thailand and China), An. maculatus (Lao and Thailand), and An. umbrosus (Lao). An minimus (Thailand Myanmar Border), Meanwhile, permethrin and deltamethrin were on An. aconitus, and An. kochi (Lao). Lastly, lambda cyalothrin and deltamethrin were on An. sundaicus (Sri Lanka), with MR ≤ 97% indicating resistance-possibility based on the WHO classification.

Table 4 shows the level of anopheles resistance to organochlorine (dichlorodiphenyltrichloroethane; DDT), organophosphate (malathion), carbamate (bendiocarb and propoxur), and pyrethroid (permethrin, deltamethrin, lambda cyalothrin, cyfluthrin, and etofenprox). Almost all the species of this mosquito studied were possibly resistant to DDT. Furthermore, this similar issue has been reported in An. stepensi, An. superpictus, An. culicifacies, An. vagus, An. sinensi, An. subpictus, and An. sachrovi to malathion. Also, it was found in An. superpictus and An. sachrovi to propoxur as well as in An. umbrosus to permethrin. The same was in An. sinensis, An. superpictus, An. sundaicus, An. minimus, An. maculatus and An. jamessi to deltamethrin. Resistance was also reported in An. stephensi, An. culcifacies, An. vagus, and An. barbirostris to permethrin and deltamethrin, and in An. stephensi to etofenprox. However, direct resistance was found in An. hyrcanus to Permethrin and deltamethrin, as well as in An. culicifacies to lambda cyalothrin. Also, this was found in An. stephensi, An. sinensis and An. culicifacies to cyfluthrin.

Table 4. Anopheles mortality rates in insecticide resistance bioassays.

NoAnopheles
species
Percentage of mortality (Susceptibility Status)Reference
OrganochlorineOrganophosphateCarbamatePyrethroid
DDT (%)Malathion (%)Bendiocarb
(%)
Propoxur
(%)
Permethrin
(%)
Deltamethrin
(%)
Lambda-
cyhalothrin
(%)
Cyfluthrin
(%)
Etofenprox
(%)
1An. stephensi*31-60 (R)47-97 (R)87-100 (PR)NA87-91 (PR)66-78 (R)20
45 (R)NANANA92.3 (PR)96(PR)88.4 (PR)55 (R)91 (PR)26
62 (R)NANANANA96 (PR)89 (PR)82 (PR)100 (S)25
2An. superpictus*50-86.7 (R-PR)61.7-88.3 (R-PR)68.3-91.7
(R-PR)
NANANANANA31
100 (S)100 (S)92 (PR)NA100 (S)85 (PR)NANANA20
3An. culicifacies*6.6-26.6 (R)65.4-100 (R-S)NANANA71.6-94.1 (R-PR)NANANA8
11.4-15.3 (R)60.4-76.2 (R)NANANA72.6-84 (R-PR)NANANA19
37.1 (R)74 (R)NANA91.3 (PR)83.8 (PR)59.9 (R)70.2 (R)NA22
81 (PR)95 (PR)100 (S)89 (PR)64(R)20
4An. annularis11.9-28.3 (R)NANANANA97.7-98.1(PR-S)NANANA21
NANANANANANANANANA23
100 (S)24
5An. minimus*NANANANANANANANANA23
NANANANANA92 (PR)NANANA24
98-100 (S)NANANA100 (S)100 (S)NANANA27
6An. hyrcanus*57 (R)NANANA48 (R)33 (R)NANANA24
72-83 (R-PR)NANANA65-87 (R-PR)45-85 (R-PR)NANANA17
90 (PR)NANANANANANANANA27
7An. barbirostris*69 (R)NANANANA97-100 (PR-S)NANANA17
74 (R)NANANA84 (PR)72 (R)NANANA24
8An. vagus*34-61 (R)NANANA89-95 (PR)79-95 (R-PR)NANANA27
67.1-88.8 (R-PR)77.3-88.9 (R-PR)NANANANANANANA28
97 (PR)NANANA95 (PR)75 (R)NANANA24
NANANANANA97.9-100 (S)NANANA28
NANANANANA100 (S)NANANA17
9An. maculatus*86-100 (PR-S)NANANANANANANANA27
NANANANA97 (PR)85 (PR)NANANA24
NANANANANA100 (PR)NANANA27
NANANANANA100 (PR)NANANA17
10An. jamessiNANANANANA87 (PR)NANANA24
11An. nivipes0-100 (R-S)NANANA90-100 (PR)100 (S)NANANA27
NANANANA100 (S)NANANANA17
12An. philippinenses33-100 (R-S)NANANA100 (S)NANANANA27
100 (S)NANANA100 (S)100 (S)NANANA17
13An. umbrosus63 (R)NANANA86 (PR)100 (S)NANANA27
14An. sinensis*30.4 (R)86.6 (PR)NANANA35.8 (R)NA32.4 (R)NA29
72.7-78.4 (R)NANANANA85.8-91(PR)NANANA28
15An. subpictus*16-35 (R)49-69 (R)NANANA82-96 (PR)72-97 (R-PR)NANA30
16An. sacharovi*55-78.3(R)58.3-90 (R-PR)NA68.3-90
(R-PR)
NANANANANA31
17An.scanloni84 (PR)NANANANANANANANA24
18An.kochi82-100 (PR-S)NANANA100 (S)100 (S)NANANA27
NANANANANA98 (S)NANANA24
19An.tessellatus14 (R)NANANA100 (S)NANANANA27
NANANANANA98 (S)NANANA24
20An.sundaicus38-47 (R)93-98 (PR-S)NANANA97-100 (S)100 (S)NANA30
21An.aconitus100 (S)NANANA100 (S)100 (S)NANANA27
22An.dirusNANANANA100 (S)NANANA17
23An.karwariNANANANA100 (S)NANANA17

*Main vector

DDT=dichlorodiphenyltrichloroethane. NA=not available, S=Susceptible (90-97% mortality suggest), P=Possible Resistance, R=Resistance= < 90%.

Table 5 shows that the insecticide resistance management strategies in several Asian countries are through vector control by environmental, biological, and chemical interventions. The implementation of chemical interventions is through insecticide rotation, monitoring their bioefficacy, mapping, and surveillance of malaria vectors. Malaria eradication relies on effective prevention, technical capability approaches, government and community support, funding sources, accurate data, and adequate implementation.

Table 5. Insecticide resistance management strategies based on Anopheles habitat.

CountryStudy locationhabitatInsecticide resistance strategiesReference
AfganistanNangarhar, Laghman, Kunar, Ghazni, and
Badakhshan
Rice field, river stream,
ponds, and water puddle
Establishing a management plan for insecticide resistance, and
monitoring this situation in all malaria-endemic provinces.
20
IndiaMadhya PradeshForestResistance management strategy by appropriate rotation of different
insecticides, including carbamates and incorporating a synergist with
synthetic pyrethroids for treating mosquito nets for the control of
malaria vectors in these areas. Periodical monitoring of susceptibility/
resistance status of different insecticides.
8,19,21,22
Asom-Meghalaya border area, northeast
India
Forest, ponds irrigation
Rayagada, Nowrangpur, Kalahandi,
Malkangiri and Koraput
Cattle sheds, human
dwelling
Gadchiroli districtForest
ThailandChiang Mai-Chiang Dao, Mae Hongsom,
Phrae
Paddy fields and rivuletVector prevention strategies and monitoring insecticide resistance.
Achieving universal coverage and proper use of LLIN for all people at
risk of malaria. Alternative control tools (e.g., insecticide-treated clothes,
spatial repellents, or treated hammocks) adapted to the situation of
people's activities are more effective in reducing the malaria burden
17,23,24
Thailand-Myanmar BorderAgriculture
Khong Chiam, Sirindhorn, Buntharik, and
Nachaluay
Forest and rice field
IranChabahar Seaport, southeast corner of IranSeaportBiological, chemical, and environmental management. Rotation of
insecticide. Monitoring and mapping of insecticide resistance in
the primary malaria vector for the implementation of any vector
control. Evaluation of the mechanisms and implementation of proper
insecticide resistance management strategies.
25,26
Sistan and BaluchistanCoastal
LaoPhongsaly, Bokeo, LuangPrabang,
Vientiane Pro, Borlikhamxay, Khammouane,
Savannakhet, Saravane, Sekong, Attapeu.
Forest, villageRoutine monitoring of the insecticide resistance levels and mechanisms
to ensure effective malaria control.
Use of insecticide with different modes of action, rotation, or
combination in the same area.
27
ChinaHainan IslandMountainous and
ricefield
Cost-effective integrated vector control programs that are beyond
synthetic insecticides. The genetic basis of insecticide resistance to
implementing more effective vector control strategies. Monitoring the
efficacy of common insecticide and exploring the molecular basis of
resistance.
28,29
Shandong ProvinceIrrigated ricefield,
aquatic habitat, and
small ponds
Sri LankaBatticaloa, Puttalam, Trincomalee and
Ampara
Coastal and inlandMonitoring genetically different vector populations and their sensitivity
to varying insecticides. Developing simple molecular tools and
techniques to differentiate morphologically similar Anopheles species
on the field.
30
TurkeySoutheastern Anatolia and the
Mediterranean
Agricultural, ponds,
stream, and swamps
Effective management of insecticide resistance and monitoring of
the status at a regular interval to prevent delay to its development.
Integrated vector control strategies including biological, chemical, and
physical strategies implemented in a combination
31

Discussion

Study sites

Ecologically, the sites used were mountainous, harbor/seaport, mixed thicket/ lush and dense forests, humid climate, rivers, rice fields, and ponds that provide a suitable environment for vector mosquito breeding. Anopheles mosquitos' seasonal activity differs in various regions due to environmental conditions24. Also, those collected were identified for species based on their morphological characteristics19,21.

Type of insecticides

Almost all Anopheles in this study were reported to be resistant to DDT. Malathion (organophosphate) is still quite effective on Anopheles sundaicus 93% in Sri Lanka and Anopheles superpictus 100% in Afghanistan. Carbamate are still quite effective for Anopheles superpictus 92% in Afghanistan. Pyrethroids were still quite effective with a range of 97–100% in An. superpictus (Afghanistan), An. maculatus (Lao and Thailand), An. nivipes (Lao and Thailand), An. philipinenses (Lao and Thailand), An. minimus, An. kochi, An. teselatus and An. aconitus (Lao), An. karwari and An. vagus (Thailand) and An. annularis (Thailand-Myanmar border). The application of chemical insecticides is one of the most critical interventions for malaria control, which included organochlorines (DDT, dieldrin, and BHC), organophosphates (pyrimytophos-methyl and malathion), carbamates (propoxur), and pyrethroids (lambda-cyhalothrin and deltamethrin). These chemicals were used in various forms of application, such as indoor residual spraying (IRS) and insecticide-treated mosquito nets (ITNS) for controlling adult mosquitos. In contrast, organophosphates for larviciding were used in malaria-prone areas25. Actually, the pyrethroids were used in various Asia countries for ITNs and long-lasting insecticidal nets (LLINs). They were also considered the most effective because of their advantages, namely low mammalian toxicity, rapid knockdown activity, and high efficacy against a wide range of insect pests, especially mosquitos25.

Insecticide resistance level frequencies

Resistance to various insecticide, especially to DDT and pyrethtoids, was common problem in different malaria vector species32. The multiple resistance to organochlorine, organophosphate and pyrethroid in this study was reported in An. stephensi (Afghanistan) and An. culicifacies (India). An. hyrcanus and An. barbirostris (Thailand-Myanmar border) and An. sinensis (China) were multiple resistant to organochlorines and pyrethroids, while An. subpictus in Sri Lanka was multiple resistant to organochorine and organophosphate. In Turkey, An. superpictus is multiple resistant to organochlorines, organophosphates and carbamates.This multiple resistance was reported in 14 malaria vector in Asia; these included: An. stephensi, An. superpictus, An. culinary, An. annularis, An. minimus, An. hyrcanus, An. barbirostris, An. vagus, An. maculatus, An. jamessi, An. nivipes, An. philippinensis, An. umbrosus, and An. sinensis. Most of the new reports were towards pyrethroid compounds, the only insecticides used for LLINs25. It represents a growing challenge for malaria control and elimination in the future. Using the same insecticide for multiple successive IRS cycles may not be recommended; it is preferable to use a rotation system with different groups of insecticides, including carbamates33. Rotations should start with the insecticides to which there is the lowest frequency of resistance. In high coverage areas with LLINs, pyrethroids may not be a good option for IRS, as this will add to selection pressure; preferably a rotation system with various types of these groups, including carbamates, should be used33. The rotation should start with an insecticide that has the lowest resistance frequency. In high-coverage areas with LLINs, pyrethroids were good choices for IRS because this added to the selection pressure. Both LLINs and IRS are the most effective insecticides where the local vectors are endophagic and endophilic. But, when the local vectors primary exophagic and exophilic, these interventions still need an essensial level of control3.

Furthermore, an insecticide mixture was a better choice for malaria vector resistance and insecticide resistance management. For example Long-lasting Insecticidal Net (LLIN) incorporating permethrin and a synergist, piperonyl butoxide (PBO), into its fibers in order to counteract metabolic-based pyrethroid resistance of Anopheles gambiae s.s. mosquitoes34. The efficacy of mixed nets, is because it prevents mosquito bites (function of resistance and physical integrity), and kills mosquitoes (function of chemical content and mosquito susceptibility)35. Resistance has been observed in more than 500 insect species worldwide, among which over 50 Anopheles species (Diptera: Culicidae) are responsible for the transmission of malaria parasites to humans36. Since monitoring of the resistance was a critical element for implementing insecticide-based vector control interventions, there was a need for periodic surveillance at least once a year or preferably every six months13. to strengthen the evidence base for the effectiveness of ongoing vector control interventions19. A new insecticide, Sumishield (clothianidin, neonicotinoid) was prequalified for indoor residue spraying by the WHO in 2017, could be an alternative in dealing with multiple insecticide-resistant Anopheles37

Mortality rates of the Anopheles populations

The susceptibility and resistance to insecticides are defined based on testing of vector mortality exposure to discriminatory doses: 1) Susceptibility: an observation of more than or equal to the mortality rate of 98% among vectors tested for resitance provides evidence of clear sustainability; 2) Possible resistance: an initial observations of less than 98% of vector mortality in bioassay carried out shows possible resistance. After this observation is made, further testing is needed to confirm resistance. Additional tests must be done to determine whether the vector mortality rates are consistently lower than 98% and to understand resistance levels32. All vectors had resistance to DDT with a value below 80%; however, the use of insecticide began to decline gradually over the last few decades and was removed entirely from malaria control in 2000. This decline was due to the perceived adverse effects on the environment and decreased public acceptance for spraying indoor residues23.

Pyrethroids were the most commonly used insecticides for ITN and IRS, which target indoor transmission and mosquitos that bite in the room28. The mortality rate was <80% for the pyrethroid group in An. vagus, An. culinary, An. stephensi, An. hyrcanus, An. barbirostris, An. superpictus, An. sacharovi, and An. subpictus. This proved that pyrethroid was less effective. Meanwhile, insecticide resistance was present in malaria vectors in Asia, and the genes spread rapidly throughout the world38. Mosquitoes have two acetylcholinesterase genes (ace-1 and ace-2), but only ace-1 was found to be significantly associated with insecticide resistance28. High insecticide resistance due to insensitive acetylcholinesterase (AChE) has emerged in genes spread of mosquitoes39. In Africa, sublethal doses of pyrethroids for parasite resistance Plasmodium falciparum and An. gambiae s.s. can interfere with parasite development in mosquitoes, significantly reducing the proportion of infected mosquitoes and the intensity of infection. This mechanism could enable pyrethroid-treated bed nets to prevent malaria transmission despite increased vector resistance40. As resistance genes spread from province to province and country to country, it is of course meaningful and very useful to observe whether and how much this spread is accompanied by an increase in routine reports of malaria incidence as recorded in local health facilities37

Interventions

Several countries in Asia are implementing an insecticide resistance management (IRM) strategy against malaria vectors following the Global Plan for IRM; this will be more effective with the support of national health system policies and cross-sectoral coordination to achieve malaria-free targets 2030. The use of insecticides to reduce vector populations has become the main strategy for malaria control. Presently, 12 of these insecticides belonging to four chemical classes are recommended by the WHO Pesticide Evaluation Scheme (WHOPES) for IRS41. The nine insecticides used in Asia which recommended by WHO are Bendiocarb, Propoxur, DDT, Malathion, α-Cypermetrhrin, Cyfluthrin, Deltamethrin, Etofenprox, and Lambda-Cyhalothrin. Current strategies for controlling malaria vectors mainly include IRS with synthetic DDT/pyrethroids and durable LLINs14. WHO recommends that these insecticides' susceptibility status needs to be monitored annually13. However, the last two decades have seen the use of insecticides everywhere, especially pyrethroids, causing widespread resistance and compromising the effectiveness of vector control42. Besides, when this situation is detected, the intensity, biochemical and molecular mechanisms should also be investigated. The accurate information about the underlying resistance mechanism and its intensity or frequency in the malaria vector turns to update the vector control program and ensure the timely management of insecticide resistance32. Therefore, biochemical and molecular tests are recommended to understand the mechanism of pyrethroid resistance, and there have been several reports about this situation in malaria vectors. However, several control strategies are used to overcome resistance, such as rotation, mixture, using biological control, and integrated vector management26.

Limitations

This study had limitations, such as the dissimilar variables investigated, which produced an incomplete analysis. Only 15 articles from eight countries that correlated with the inclusion criteria from the selected ten years of studies. The data on each country's mortality rate presented only the smallest value, therefore, making it difficult to explore the whole data that needed to make the discussion complete. In some countries, the bioassay test did not use carbamate, even though it was effective for controlling certain types of Anopheles.

Conclusion

This review found organochlorine (DDT), organophosphate (malathion), and pyrethroids resistance in several Anopheles species with a less than 80% mortality rate. The reports of pyrethroid resistance were quite challenging because it is considered effective in the malaria vector control. Several countries in Asia are implementing an insecticide resistance management (IRM) strategy against malaria vectors following the Global Plan for IRM. Intervention and implementation with optimal resource support are carried out in several Asian countries, including the management plans in selecting insecticides, using a rotation system during interventions in the field, regular monitoring, and integrating vector control based on physics, chemistry, and biology. Several strategies are needed, including management plans in selecting insecticides, using a rotation system during the field interventions, regular monitoring, and integrating vector control strategies based on physical, chemical, and biological methods. All these need to be supported by cross-sector policies and cooperation to achieve the 2030 malaria-free target.

Data availability

Underlying data

All data underlying the results are available as part of the article and no additional source data are required.

Extended data

Figshare: PRISMA 2009 checklist for an article entitled Current status of insecticide resistance in malaria vectors in the Asian countries: systematic review. https://doi.org/10.6084/m9.figshare.1358607815.

This project contains the following extended data:

  • - PRISMA flow diagram of systematic review inclusion and exclusion process

Reporting guidelines

Figshare: PRISMA checklist for ‘Current status of insecticide resistance in malaria vectors in the Asian countries: systematic review’. https://doi.org/10.6084/m9.figshare.1358251712.

Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0).

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Susanna D and Pratiwi D. Current status of insecticide resistance in malaria vectors in the Asian countries: a systematic review [version 2; peer review: 1 approved, 2 approved with reservations]. F1000Research 2022, 10:200 (https://doi.org/10.12688/f1000research.46883.2)
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Reviewer Report 28 Jan 2022
Manaswini Dehuri, Department of Veterinary Parasitology, College of Veterinary Science and Animal Husbandry, orissa university of agriculture & technology, Bhubaneswar, India 
Approved with Reservations
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The scope of the article is good and it is a relevant topic. There are grammatical mistakes and many sentences needs to be rewritten in the article e.g.:
  • The 2nd line of introduction needs to be
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Dehuri M. Reviewer Report For: Current status of insecticide resistance in malaria vectors in the Asian countries: a systematic review [version 2; peer review: 1 approved, 2 approved with reservations]. F1000Research 2022, 10:200 (https://doi.org/10.5256/f1000research.78974.r118553)
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Reviewer Report 26 Jan 2022
Josiane Etang, Organization for Coordination of the Fight Against Endemic Diseases in Central Africa (OCEAC), Yaoundé, Cameroon;  Faculty of Medicine and Pharmaceutical Sciences, University of Douala, Douala, Cameroon 
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Most of the comments made on the previous version of the manuscript have been addressed. However, there is ... Continue reading
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Etang J. Reviewer Report For: Current status of insecticide resistance in malaria vectors in the Asian countries: a systematic review [version 2; peer review: 1 approved, 2 approved with reservations]. F1000Research 2022, 10:200 (https://doi.org/10.5256/f1000research.78974.r118541)
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Reviewer Report 01 Oct 2021
Charles M. Mbogo, Kenya Medical Research Institute-Wellcome Trust Research Program, Nairobi, Kenya 
Approved with Reservations
VIEWS 15
The authors are reporting on insecticide resistance data compiled through systematic review from Asian countries. The purpose of this systematic review was to understand the current status of insecticide resistance among malaria vectors and the implementation of the interventions.
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Mbogo CM. Reviewer Report For: Current status of insecticide resistance in malaria vectors in the Asian countries: a systematic review [version 2; peer review: 1 approved, 2 approved with reservations]. F1000Research 2022, 10:200 (https://doi.org/10.5256/f1000research.49960.r93580)
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Reviewer Report 30 Jun 2021
Josiane Etang, Organization for Coordination of the Fight Against Endemic Diseases in Central Africa (OCEAC), Yaoundé, Cameroon;  Faculty of Medicine and Pharmaceutical Sciences, University of Douala, Douala, Cameroon 
Approved with Reservations
VIEWS 22
The emergence and spread of Anopheles resistance to insecticides is a growing issue, that jeopardizes the effectiveness of currently available core malaria vector control tools, i.e. Long Lasting Insecticidal nets (LLINs) and Indoor Residual Spraying (IRS).

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Etang J. Reviewer Report For: Current status of insecticide resistance in malaria vectors in the Asian countries: a systematic review [version 2; peer review: 1 approved, 2 approved with reservations]. F1000Research 2022, 10:200 (https://doi.org/10.5256/f1000research.49960.r87116)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.

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Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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