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

Dewi Susanna; Dian Pratiwi

doi:10.12688/f1000research.46883.1

Home Browse Current status of insecticide resistance in malaria vectors in the...

ALL Metrics

-

Views

-

Downloads

Get PDF

Get XML

Export

▬

✚

Systematic Review

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

[version 1; peer review: 2 approved with reservations]

Dewi Susanna ¹, Dian Pratiwi²

PUBLISHED 10 Mar 2021

Author details Author details

¹ Department of Environmental Health, Faculty of Public Health, Universitas Indonesia, Depok, Jawa Barat, 16424, Indonesia
² Alumni of Faculty of Public Health, Universitas Indonesia, Depok, Jawa Barat, 16424, Indonesia

Dewi Susanna
Roles: Conceptualization, Funding Acquisition, Methodology, Project Administration, Resources, Supervision, Validation, Visualization, Writing – Original Draft Preparation, Writing – Review & Editing

Dian Pratiwi
Roles: Data Curation, Formal Analysis, Investigation, Methodology, Visualization, Writing – Original Draft Preparation

OPEN PEER REVIEW

REVIEWER STATUS

Abstract

Background: The application of insecticides for malaria vector control has remained a global problem, due to the current trend of increased resistance against these chemicals. This study aims to determine the insecticide-resistant status 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 dichlorodiphenyltrichloroethane (DDT) and pyrethroids resistance in several anopheles species with a mortality rate of less than 80%.
Conclusions: The report on the pyrethroid resistance was complicated, since this insecticide was considered effective in malaria vector control. Therefore, several strategies were required, 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. All of these need to be supported by cross-sector policies and cooperation in achieving the 2030 malaria-free target.

Keywords

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

Corresponding author: Dewi Susanna

Competing interests: No competing interests were disclosed.

Grant information: This manuscript was funded by the Directorate of Research and Community Engagement Universitas Indonesia through Indexed International Publication for QQ scheme Contract No. NKB-0260/UN2.R3.1/HKP. 05.00/2019.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2021 Susanna D and Pratiwi D. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Data associated with the article are available under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original data is properly cited.

How to cite: Susanna D and Pratiwi D. Current status of insecticide resistance in malaria vectors in the Asian countries: a systematic review [version 1; peer review: 2 approved with reservations]. F1000Research 2021, 10:200 (https://doi.org/10.12688/f1000research.46883.1) First published: 10 Mar 2021, 10:200 (https://doi.org/10.12688/f1000research.46883.1) Latest published: 04 Jan 2022, 10:200 (https://doi.org/10.12688/f1000research.46883.2)

Introduction

Malaria is one of the most common vector-borne diseases widespread in the tropics and subtropics¹. According to the World Malaria Report (2019), an estimated 219 million cases were recorded in 2017, compared to the 217 million in the previous year². 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 mainly depends on one class of insecticides, namely pyrethroids; however, the increase in resistance to it reduces this treatment's efficacy⁵. The progressive reduction of malaria's burden through substantial improvements of insecticide-based vector control in recent years is 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 this type of organism. 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 monitoring regular 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, publishing year, the country where it was conducted, settings, location characteristics, bioassay methods, the sample of Anopheles mosquito, and the quartiles in SCImagoJR. SCImagoJR is a publicly available portal that includes the journals and country scientific indicators developed from the information contained in the Scopus database. The findings were arranged according to the objective and result 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. 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

The identification process for review is outlined 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.

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 characteristics.

Authors	Title	Publish	Country	Study periods	Publisher	Reference
Ahmad et al.	Status of insecticide resistance in high-risk malaria provinces in Afghanistan.	2016	Afghanistan	August to October 2014	Malaria Journal	24
Mishra et al.	Insecticide resistance status of Anopheles culicifacies in Madhya Pradesh, central India	2012	India	August to September 2009	Journal 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	2014	India	June–August 2011	Journal of Vector- Borne Diseases	21
Sahu et al.	Triple insecticide resistance of Anopheles culicifacies: A practical impediment for malaria control in Odisha State, India.	2015	India	April to June 2014	Indian Journal of Medical Research	19
Chand et al.	Insecticide resistance status of An. culicifacies in Gadchiroli (Maharashtra) India	2017	India	August 2016 and February 2017	Pathogens and global health	25
Chareonviriyaphap et al.	Review of insecticide resistance and behavioral avoidance of human diseases by vectors in Thailand	2013	Thailand	2000–2010	Parasites & Vectors	26
Chaumeau et al.	Insecticide resistance of malaria vectors along the Thailand-Myanmar border	2017	Thailand	August and November 2014, July 2015	Parasites & Vectors	20
Sumarnrote et al.	Insecticide resistance status of Anopheles mosquitoes in Ubon Ratchathani province, Northeastern Thailand	2017	Thailand	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	2018	Iran	April–June 2015	Journal of Arthropod-Borne Diseases	22
Vatandoost et al.	Indication of pyrethroid resistance in the main malaria vector, Anopheles stephensi from Iran	2012	Iran	Spring 2011	Asian Pacific Journal of Tropical Medicine	27
Marcombe et al.	Insecticide resistance status of malaria vectors in Lao PDR	2017	Lao	The rainy (June to October) and dry (January to May) seasons of 2014 and 2015	PloS One	28
Qin et al.	Insecticide resistance of Anopheles sinensis and An. vagus in Hainan Island, a malaria-endemic area in China	2014	China	July–August 2012	Parasites & Vectors	29
Dai et al.	Development of insecticide resistance of malaria vector Anopheles sinensis in Shandong Province In China	2015	China	2003–2012	Malaria Journal	30
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	2012	Sri Lanka	July 2008–June 2010	Parasites & Vectors	31
S.İ. Yavaşoglu, et al.	Current insecticide resistance status of Anopheles sacharovi and A. superpictus in former malaria-endemic areas of Turkey	2019	Turkey	April 2014 and September 2015	ActaTropica	32

There were 23 species of Anopheles from these studies (Table 2). In several countries, 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 malaria vector was divided into three habitats, based on distribution, namely in rice fields, forests and on the coast, and flowing rivers. 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. Sample and location characteristics.

Study location	Country	Anopheles species	Sample adult female mosquitos (n)	Vector habitat	Reference
Nangarhar, Laghman, Kunar, Ghazni, and Badakhshan	Afghanistan	An. stephensi, An. superpictus, An. culicifacies	2049	Ricefield, river stream, ponds, and water puddle	24
Madhya Pradesh	India	An. culicifacies	NA	Forest	8
Asom-Meghalaya border area, northeast India	India	An. annularis	200	Forest, ponds irrigation	21
Rayagada, Nowrangpur, Kalahandi, Malkangiri and Koraput	India	An. culicifacies	1740	Forest	19
Gadchiroli district	India	An. culicifacies	NA	Forest	25
Chiang Mai-Chiang Dao, Mae Hongsom, Phrae	Thailand	An. minimus An. annularis	NA	Paddy fields and rivulet	26
Thailand-Myanmar Border	Thailand	An. annularis, An. minimus, An. hyrcanus, An. barbirostris, An. vagus, An. maculatus, An. jamessi, An. scanloni, An. kochi, An. tesselatus	5896	Agriculture	20
Khong Chiam, Sirindhorn, Buntharik, and Nachaluay	Thailand	An. hyrcanus, An. barbirostris, An. maculatus, An. nivipes, An. philipinensis, An. vagus An. dirus An. karwari	2088	Forest and ricefield	17
Chabahar Seaport, southeast corner of Iran	Iran	An. stephensi	317	Seaport	22
Sistan and Baluchistan	Iran	An.stephensi	733	Coastal	27
Phongsaly, Bokeo, LuangPrabang, Vientiane Pro, Borlikhamxay, Khammouane, Savannakhet, Saravane, Sekong, Attapeu.	Lao	An. minimus, An. hyrcanus, An. vagus An. maculatus An. nivipes An. philipinesnis An. umbrosus An. kochi An. tesselatus An. aconitus	3977	Forest, village, agriculture	28
Hainan Island	China	An. sinensis, An. vagus	1468	Mountainous and ricefield	29
Shandong Province	China	An. sinensis	4370	Irrigated ricefield, aquatic habitat, and small ponds	30
Batticaloa, Puttalam, Trincomalee and Ampara	Sri Lanka	An. subpictus An. sundaicus	256	Coastal and inland	31
Southeastern Anatolia and the Mediterranean	Turkey	An. superpictus, An. sacharovi	1230	Agricultural, ponds, stream and swamps	32

The entire female Anopheles collected was morphologically identified for their species or complexes using stereomicroscopes and morphological keys¹⁶. The mosquitoes were separated into groups of species, complexes, or bioassay, then 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 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% was prepared by adopting the WHO standard method¹⁴ (Table 3).

Table 3. WHO bioassay method.

Country	WHO bioassay with insecticides
	Organochlorine	Organophosphate	Carbamate		Pyrethroid
	DDT (%)	malathion (%)	Bendiocarb (%)	Propoxur (%)	Permethrin (%)	Deltamethrin (%)	Lambda- cyhalothrin (%)	Cyfluthrin (%)	Etofenprox (%)
Afghanistan	4.0	5.0	0.1	NA	0.75	0.05	NA	NA	NA
India	4.0	5.0	NA	NA	NA	0.05	NA	NA	NA
India	4.0	NA	NA	NA	NA	0.05	NA	NA	NA
India	4.0	5.0	NA	NA	NA	0.05	NA	NA	NA
India	4.0	NA	NA	NA	0.75	0.05	0.05	0.15	NA
Thailand	4.0	NA	NA	NA	NA	NA	NA	NA	NA
Thailand	4.0	NA	NA	NA	0.75	0.05	NA	NA	NA
Thailand	4.0	NA	NA	NA	0.75	0.05	NA	NA	NA
Iran	4.0	NA	NA	NA	0.75	0.05	0.05	0.15	0.5
Iran	4.0	NA	NA	NA	0.75	0.05	0.05	0.15	0.5
Lao	4.0	NA	NA	NA	0.75	0.05	NA	NA	NA
China	4.0	5.0	NA	NA	NA	0.05	NA	NA	NA
China	4.0	5.0	NA	NA	NA	0.05	NA	0.15	NA
Sri Lanka	4.0	5.0	NA	NA	NA	0.05	0.05	NA	NA
Turkey	4.0	5.0	NA	0,1	0,75	0,05	NA	NA	0.5

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. Bioassay results were summarized in three resistance classes according to the WHO criteria¹²: (1) susceptible when death was 98% or higher, (2) resistance-possibility was tolerable when mortality was between 97% and 80%, and (3) resistant when death case was lower than 80%¹⁸.

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. Mortality rate of insecticide resistance bioassay in Anopheles.

No	Anopheles species	Percentage of mortality (Susceptibility Status)									Reference
		Organochlorine	Organophosphate	Carbamate		Pyrethroid
		DDT (%)	Malathion (%)	Bendiocarb (%)	Propoxur (%)	Permethrin (%)	Deltamethrin (%)	Lambda- cyhalothrin (%)	Cyfluthrin (%)	Etofenprox (%)
1	An. stephensi^*	31-60 (R)	47-97 (R)	87-100 (PR)	NA	87-91 (PR)	66-78 (R)				24
		45 (R)	NA	NA	NA	92.3 (PR)	96(PR)	88.4 (PR)	55 (R)	91 (PR)	27
		62 (R)	NA	NA	NA	NA	96 (PR)	89 (PR)	82 (PR)	100 (S)	22
2	An. superpictus^*	50-86.7 (R-PR)	61.7-88.3 (R-PR)		68.3-91.7 (R-PR)	NA	NA	NA	NA	NA	32
2	An. superpictus^*	100 (S)	100 (S)	92 (PR)	NA	100 (S)	85 (PR)	NA	NA	NA	24
3	An. culicifacies^*	6.6-26.6 (R)	65.4-100 (R-S)	NA	NA	NA	71.6-94.1 (R-PR)	NA	NA	NA	8
		11.4-15.3 (R)	60.4-76.2 (R)	NA	NA	NA	72.6-84 (R-PR)	NA	NA	NA	19
		37.1 (R)	74 (R)	NA	NA	91.3 (PR)	83.8 (PR)	59.9 (R)	70.2 (R)	NA	25
		81 (PR)	95 (PR)	100 (S)		89 (PR)	64(R)				24
4	An. annularis	11.9-28.3 (R)	NA	NA	NA	NA	97.7-98.1(PR-S)	NA	NA	NA	21
		NA	NA	NA	NA	NA	NA	NA	NA	NA	26
							100 (S)				20
5	An. minimus^*	NA	NA	NA	NA	NA	NA	NA	NA	NA	26
		NA	NA	NA	NA	NA	92 (PR)	NA	NA	NA	20
		98-100 (S)	NA	NA	NA	100 (S)	100 (S)	NA	NA	NA	28
6	An. hyrcanus^*	57 (R)	NA	NA	NA	48 (R)	33 (R)	NA	NA	NA	20
		72-83 (R-PR)	NA	NA	NA	65-87 (R-PR)	45-85 (R-PR)	NA	NA	NA	17
		90 (PR)	NA	NA	NA	NA	NA	NA	NA	NA	28
7	An. barbirostris^*	69 (R)	NA	NA	NA	NA	97-100 (PR-S)	NA	NA	NA	17
7	An. barbirostris^*	74 (R)	NA	NA	NA	84 (PR)	72 (R)	NA	NA	NA	20
8	An. vagus^*	34-61 (R)	NA	NA	NA	89-95 (PR)	79-95 (R-PR)	NA	NA	NA	28
		67.1-88.8 (R-PR)	77.3-88.9 (R-PR)	NA	NA	NA	NA	NA	NA	NA	29
		97 (PR)	NA	NA	NA	95 (PR)	75 (R)	NA	NA	NA	20
		NA	NA	NA	NA	NA	97.9-100 (S)	NA	NA	NA	29
		NA	NA	NA	NA	NA	100 (S)	NA	NA	NA	17
9	An. maculatus^*	86-100 (PR-S)	NA	NA	NA	NA	NA	NA	NA	NA	28
		NA	NA	NA	NA	97 (PR)	85 (PR)	NA	NA	NA	20
		NA	NA	NA	NA	NA	100 (PR)	NA	NA	NA	28
		NA	NA	NA	NA	NA	100 (PR)	NA	NA	NA	17
10	An. jamessi	NA	NA	NA	NA	NA	87 (PR)	NA	NA	NA	20
11	An. nivipes	0-100 (R-S)	NA	NA	NA	90-100 (PR)	100 (S)	NA	NA	NA	28
11	An. nivipes	NA	NA	NA	NA	100 (S)	NA	NA	NA	NA	17
12	An. philippinenses	33-100 (R-S)	NA	NA	NA	100 (S)	NA	NA	NA	NA	28
12	An. philippinenses	100 (S)	NA	NA	NA	100 (S)	100 (S)	NA	NA	NA	17
13	An. umbrosus	63 (R)	NA	NA	NA	86 (PR)	100 (S)	NA	NA	NA	28
14	An. sinensis^*	30.4 (R)	86.6 (PR)	NA	NA	NA	35.8 (R)	NA	32.4 (R)	NA	30
14	An. sinensis^*	72.7-78.4 (R)	NA	NA	NA	NA	85.8-91(PR)	NA	NA	NA	29
15	An. subpictus^*	16-35 (R)	49-69 (R)	NA	NA	NA	82-96 (PR)	72-97 (R-PR)	NA	NA	31
16	An. sacharovi^*	55-78.3(R)	58.3-90 (R-PR)	NA	68.3-90 (R-PR)	NA	NA	NA	NA	NA	32
17	An.scanloni	84 (PR)	NA	NA	NA	NA	NA	NA	NA	NA	20
18	An.kochi	82-100 (PR-S)	NA	NA	NA	100 (S)	100 (S)	NA	NA	NA	28
18	An.kochi	NA	NA	NA	NA	NA	98 (S)	NA	NA	NA	20
19	An.tessellatus	14 (R)	NA	NA	NA	100 (S)	NA	NA	NA	NA	28
19	An.tessellatus	NA	NA	NA	NA	NA	98 (S)	NA	NA	NA	20
20	An.sundaicus	38-47 (R)	93-98 (PR-S)	NA	NA	NA	97-100 (S)	100 (S)	NA	NA	31
21	An.aconitus	100 (S)	NA	NA	NA	100 (S)	100 (S)	NA	NA	NA	28
22	An.dirus	NA	NA	NA	NA		100 (S)	NA	NA	NA	17
23	An.karwari	NA	NA	NA	NA		100 (S)	NA	NA	NA	17

*Main vector

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

Table 5 shows that insecticide resistance interventions in several Asian countries are through vector prevention by environmental, biological, and chemical management. Implementation is through insecticide rotation monitoring, mapping, and surveillance. Malaria eradication started from effective prevention, technical capability approaches, government and community support, funding sources, accurate data, and adequate implementation.

Table 5. Insecticide resistance strategies.

Country	Study location	Location characteristic	Insecticide resistance strategies	Reference
Afganistan	Nangarhar, 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.	24
India	Madhya Pradesh	Forest	Resistance 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.	8,19,21,25
	Asom-Meghalaya border area, northeast India	Forest, ponds irrigation
	Rayagada, Nowrangpur, Kalahandi, Malkangiri and Koraput	Cattle sheds, human dwelling
	Gadchiroli district	Forest
Thailand	Chiang Mai-Chiang Dao, Mae Hongsom, Phrae	Paddy fields and rivulet	Vector 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	17,20,26
	Thailand-Myanmar Border	Agriculture
	Khong Chiam, Sirindhorn, Buntharik, and Nachaluay	Forest and rice field
Iran	Chabahar Seaport, southeast corner of Iran	Seaport	Biological, 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.	22,27
Iran	Sistan and Baluchistan	Coastal
Lao	Phongsaly, Bokeo, LuangPrabang, Vientiane Pro, Borlikhamxay, Khammouane, Savannakhet, Saravane, Sekong, Attapeu.	Forest, village	Routine 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.	28
China	Hainan Island	Mountainous 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.	29,30
China	Shandong Province	Irrigated ricefield, aquatic habitat, and small ponds
Sri Lanka	Batticaloa, Puttalam, Trincomalee and Ampara	Coastal and inland	Monitoring 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.	31
Turkey	Southeastern 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	32

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 conditions²⁰. Also, those collected were identified for species based on their morphological characteristics^19,21.

Type of insecticide

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). And 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 areas²². Currently, 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 mosquitos²².

Insecticide resistance level

Resistance to various insecticide classes was a common problem in different malaria vector species. This situation has been reported and is shown in Table 5, including widespread resistance to DDT and pyrethroids²³. The multiple resistance of reported malaria vector 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 in Asia. Most of the new reports were towards pyrethroid compounds, the only insecticides used for LLINs²². This became a challenge for malaria control and elimination, therefore, using the same insecticide for multiple successive IRS cycles is not recommended; 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.

Furthermore, using an impregnated net synergistically with synthetic pyrethroid was a better choice for malaria vectors resistant to this class of chemical. The mixed nets, such as the aforementioned, have applications against resistible mosquitoes, mainly based on oxidative metabolism³⁴. 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.

Mortality rate of the Anopheles

The mortality test category was in the range between 98–100%, 80–97%, and <80%, and was categorized as susceptible, possibly resistant, and resistant population, respectively²³. 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 residues³⁵.

Pyrethroids were the most commonly used insecticides for ITN and IRS, which target indoor transmission and mosquitos that bite in the room²⁹. 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 world³⁶.

Intervention

The use of insecticides to reduce vector populations has become the main strategy for malaria control. Presently, 12 of these interventions belonging to four chemical classes are recommended by the WHO Pesticide Evaluation Scheme (WHOPES) for IRS³⁷. 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 control³⁸. 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 turn to update the vector control program and ensure the timely management of insecticide resistance²³. Therefore, biochemical and molecular tests are recommended to understand the mechanism of pyrethroid resistance, and there have been several reports about this situation in the malaria vectors. However, several control strategies are used to fight resistance, such as rotation, mixture, using biological control, and integrated vector management²⁷.

Limitations

This study had limitations, such as the dissimilar variables investigated, which produced an incomplete analysis. There were 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 need 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

The reports of pyrethroid resistance were quite focused on because it is considered effective in the malaria vector control. Several strategies are needed, including management plans in selecting insecticides, using a rotation system during the field interventions, regular monitoring, and integrating vector control based on physics, chemistry, and biology. 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).

Authors’ contributions

DS contributed in designing and conducting the study, and also writing the draft of the manuscript, while DP searched and extracted the used data from the databases. The authors analyzed, edited, read, and approved the final manuscript in the English language. DS: Funding Acquisition of the financial support for the project leading to this publication.

Acknowledgments

The authors are grateful to the Directorate of Research and Community Engagement for giving the Indexed International Publication for Project grant and financial support. Authors also would like to thank MS. Rusyda Ihwani Tantia NOVA, SKM, M.Kes for her comments for improving this work.

Faculty Opinions recommended

References

1. World Health Organization: Anopheline Species Complexes in South and South-East Asia. no. 57. 2007. Reference Source
2. World Health Organization: World malaria report 2018. Switzerland: World Health Organization, 2018. Reference Source
3. World Health Organization: Malaria Surveillance, Monitoring & Evaluation: a Reference Manual. Global Malaria Programme -WHO, 2018. Reference Source
4. Enayati A, Hemingway J: Malaria management: Past, present, and future. Annu Rev Entomol. 2010; 55: 569–591. PubMed Abstract | Publisher Full Text
5. Hemingway J, Ranson H, Magill A, et al.: Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet. 2016; 287(10029): 1785–1788. PubMed Abstract | Publisher Full Text | Free Full Text
6. Kleinschmidt I, Mnzava AP, Kafy HT, et al.: Design of a study to determine the impact of insecticide resistance on malaria vector control: A multi-country investigation. Malar J. 2015; 14: 282. PubMed Abstract | Publisher Full Text | Free Full Text
7. Kleinschmidt I, Bradley J, Knox TB, et al.: Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: a WHO-coordinated, prospective, international, observational cohort study. Lancet Infect Dis. 2018; 18(6): 640–649. PubMed Abstract | Publisher Full Text | Free Full Text
8. Mishra AK, Chand SK, Barik TK, et al.: Insecticide resistance status in Anopheles culicifacies in Madhya Pradesh, central India. J Vector Borne Dis. 2012; 49(1): 39–41. PubMed Abstract
9. Bhatt S, Weiss DJ, Cameron E, et al.: The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015; 526(7572): 207–211. PubMed Abstract | Publisher Full Text | Free Full Text
10. Kona MP, Kamaraju R, Donnelly MJ, et al.: Characterization and monitoring of deltamethrin-resistance in Anopheles culicifacies in the presence of a long-lasting insecticide-treated net intervention. Malar J. 2018; 17(1): 414. PubMed Abstract | Publisher Full Text | Free Full Text
11. PRISMA: PRISMA. [Accessed: 24-Feb-2021]. Reference Source
12. Susanna D: PRISMA 2009 check list: Current status of insecticide resistance in malaria vectors in the Asian countries: systematic review. figshare. 2021.
13. World Health Organization: Test procedures for insecticide resistance monitoring in malaria vector mosquitoes (Second edition). Second edi. Geneva, 2018. Reference Source
14. World Health Organization: Pesticides and their application, for the control of vectors and pests of public health importance, sixth edition. Department of Control of Neglected Tropical Diseases WHO Pesticide evaluation scheme (WHOPES), 2006. Reference Source
15. Susanna D: PRISMA flow diagram of systematic review inclusion and exclusion process for Current status of insecticide resistance in malaria vectors in the Asian countries. 2021; [Accessed: 24-Feb-2021]. Available: https://figshare.com/articles/figure/PRISMA_flow_diagram_of_systematic_review_inclusion_and_exclusion_process_for_Current_status_of_insecticide_resistance_in_malaria_vectors_in_the_Asian_countries_/13586078.
16. Rattanarithikul R, Harrison BA, Harbach RE, et al.: Illustrated keys to the mosquitoes of Thailand. IV. Anopheles. Southeast Asian J Trop Med Public Health. 2006; 37 Suppl 2: 1–128. PubMed Abstract
17. Sumarnrote A, Marasri N, Overgaard HJ, et al.: Status of insecticide resistance in Anopheles mosquitoes in Ubon Ratchathani province, Northeastern Thailand. Malar J. 2017; 16(1): 299. PubMed Abstract | Publisher Full Text | Free Full Text
18. Glick JI: Illustrated key to the female Anopheles of southwestern Asia and Egypt (Diptera: Culicidae). Mosq Syst. 1992; 24: 125–153. Reference Source
19. Sahu SS, Gunasekaran K, Vijayakumar T, et al.: Triple insecticide resistance in Anopheles culicifacies: A practical impediment for malaria control in Odisha state, India. Indian J Med Res. 2015; 142 Suppl(Suppl 1): S59–63. PubMed Abstract | Publisher Full Text | Free Full Text
20. Chaumeau V, Zadrozny J, Cerqueira D, et al.: Insecticide resistance in malaria vectors along the Thailand-Myanmar border. Parasit Vectors. 2017; 10(1): 165. PubMed Abstract | Publisher Full Text | Free Full Text
21. Dhiman S, Rabha B, Goswami D, et al.: Insecticide resistance and human blood meal preference of Anopheles annularis in Asom-Meghalaya border area, Northeast India. J Vector Borne Dis. 2014; 51(2): 133–136. PubMed Abstract
22. Gorouhi MA, Oshaghi MA, Vatandoost H, et al.: Biochemical Basis of Cyfluthrin and DDT Resistance in Anopheles stephensi (Diptera: Culicidae) in malarious area of Iran. J Arthropod Borne Dis. 2018; 12(3): 310–320. PubMed Abstract | Publisher Full Text | Free Full Text
23. World Health Organization: Global plan for insecticide resistance management in malaria vectors (GPIRM). France: WHO GLOBAL MALARIA PROGRAMME, 2012. Reference Source
24. Ahmad M, Buhler C, Pignatelli P, et al.: Status of insecticide resistance in high-risk malaria provinces in Afghanistan. Malar J. 2016; 15: 98. PubMed Abstract | Publisher Full Text | Free Full Text
25. Chand G, Behera P, Bang A, et al.: Status of insecticide resistance in An. culicifacies in Gadchiroli (Maharashtra) India. Pathog Glob Health. 2017; 111(7): 362–366. PubMed Abstract | Publisher Full Text | Free Full Text
26. Chareonviriyaphap T, Bangs MJ, Suwonkerd W, et al.: Review of insecticide resistance and behavioral avoidance of vectors of human diseases in Thailand. Parasit Vectors. 2013; 6: 280. PubMed Abstract | Publisher Full Text | Free Full Text
27. Vatandoost H, Hanafi-Bojd AA: Indication of pyrethroid resistance in the main malaria vector, Anopheles stephensi from Iran. Asian Pac J Trop Med. 2012; 5(9): 722–726. PubMed Abstract | Publisher Full Text
28. Marcombe S, Bobichon J, Somphong B, et al.: Insecticide resistance status of malaria vectors in Lao PDR. PLoS One. 2017; 12(4): e0175984. PubMed Abstract | Publisher Full Text | Free Full Text
29. Qin Q, Li Y, Zhong D, et al.: Insecticide resistance of Anopheles sinensis and An. vagus in Hainan Island, a malaria-endemic area of China. Parasit Vectors. 2014; 7: 92. PubMed Abstract | Publisher Full Text | Free Full Text
30. Dai Y, Huang X, Cheng P, et al.: Development of insecticide resistance in malaria vector Anopheles sinensis populations from Shandong province in China. Malar J. 2015; 14: 62. PubMed Abstract | Publisher Full Text | Free Full Text
31. Surendran SN, Jude PJ, Weerarathne TC, et al.: Variations in susceptibility to common insecticides and resistance mechanisms among morphologically identified sibling species of the malaria vector Anopheles subpictus in Sri Lanka. Parasit Vectors. 2012; 5: 34. PubMed Abstract | Publisher Full Text | Free Full Text
32. Yavaşoglu Sİ, Yaylagül EÖ, Akıner MM, et al.: Current insecticide resistance status in Anopheles sacharovi and Anopheles superpictus populations in former malaria endemic areas of Turkey. Acta Trop. 2019; 193: 148–157. PubMed Abstract | Publisher Full Text
33. Raghavendra K, Verma V, Srivastava HC, et al.: Persistence of DDT, malathion & deltamethrin resistance in anopheles culicifacies after their sequential withdrawal from indoor residual spraying in Surat district, India. Indian J Med Res. 2010; 132: 260–264. PubMed Abstract
34. Pennetier C, Bouraima A, Chandre F, et al.: Efficacy of Olyset® Plus, a New Long-Lasting Insecticidal Net Incorporating Permethrin and Piperonil-Butoxide against Multi-Resistant Malaria Vectors. PLoS One. 2013; 8(10): e75134. PubMed Abstract | Publisher Full Text | Free Full Text
35. Chareonviriyaphap T, Bangs MJ, Suwonkerd W, et al.: Review of insecticide resistance and behavioral avoidance of vectors of human diseases in Thailand. Parasit Vectors. 2013; 6: 280. PubMed Abstract | Publisher Full Text | Free Full Text
36. Ranson H, N’Guessan R, Lines J, et al.: Pyrethroid resistance in African anopheline mosquitoes: What are the implications for malaria control? Trends Parasitol. 2011; 27(2): 91–98. PubMed Abstract | Publisher Full Text
37. World Health Organization: WHO recommended insecticides for indoor residual spraying against malaria vectors. no. October, 2013; 2013. Reference Source
38. Thomsen EK, Hemingway C, South A, et al.: ResistanceSim: Development and acceptability study of a serious game to improve understanding of insecticide resistance management in vector control programmes. Malar J. 2018; 17(1): 422. PubMed Abstract | Publisher Full Text | Free Full Text

Comments on this article Comments (0)

Version 2

VERSION 2 PUBLISHED 10 Mar 2021

Author details Author details

¹ Department of Environmental Health, Faculty of Public Health, Universitas Indonesia, Depok, Jawa Barat, 16424, Indonesia
² Alumni of Faculty of Public Health, Universitas Indonesia, Depok, Jawa Barat, 16424, Indonesia

Dewi Susanna
Roles: Conceptualization, Funding Acquisition, Methodology, Project Administration, Resources, Supervision, Validation, Visualization, Writing – Original Draft Preparation, Writing – Review & Editing

Dian Pratiwi
Roles: Data Curation, Formal Analysis, Investigation, Methodology, Visualization, Writing – Original Draft Preparation

Competing interests

No competing interests were disclosed.

Grant information

This manuscript was funded by the Directorate of Research and Community Engagement Universitas Indonesia through Indexed International Publication for QQ scheme Contract No. NKB-0260/UN2.R3.1/HKP. 05.00/2019.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Article Versions (2)

version 2

Revised

Published: 04 Jan 2022, 10:200

https://doi.org/10.12688/f1000research.46883.2

version 1

Published: 10 Mar 2021, 10:200

https://doi.org/10.12688/f1000research.46883.1

Copyright

© 2021 Susanna D and Pratiwi D. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Data associated with the article are available under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original data is properly cited.

Download

Export To

metrics

	Views	Downloads
F1000Research	-	-
PubMed Central Data from PMC are received and updated monthly.	-	-

Citations

0

SEE MORE DETAILS

CITE

how to cite this article

Susanna D and Pratiwi D. Current status of insecticide resistance in malaria vectors in the Asian countries: a systematic review [version 1; peer review: 2 approved with reservations]. F1000Research 2021, 10:200 (https://doi.org/10.12688/f1000research.46883.1)

NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.

track

receive updates on this article

Track an article to receive email alerts on any updates to this article.

Open Peer Review

Version 1

VERSION 1

PUBLISHED 10 Mar 2021

Views

15

Reviewer Report 01 Oct 2021

Charles M. Mbogo, Kenya Medical Research Institute-Wellcome Trust Research Program, Nairobi, Kenya

Approved with Reservations

https://doi.org/10.5256/f1000research.49960.r93580

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.
... Continue reading

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.

Introduction/Background:

The background information is sound, and the research question is easily identifiable. However, a few minor comments:

Paragraph 2 --- “The prevention of malaria mainly depends on one class of insecticides, namely pyrethroids; however, the increase in resistance to it reduces this treatment’s efficacy”. This sentence is not clear because malaria control may be done using the 4 available classes of insecticides and not the pyrethroids unless one is talking about LLINs.
Paragraph 3 –states that “Vector control is an essential aspect of a program organized to manage the disease transmitted by this type of organism”. Be specific and state what kind of organism is this.

Methods:

The methodologies applied are appropriate and adequately described. The searching process used was also appropriate. However, the authors indicated that they selected the 15 papers based on several criteria of which one included WHO bioassay protocol on the four major insecticide classes and did not consider any other bioassay protocols such as CDC bottle assay.

Currently, insecticide resistance is measured using WHO bioassay protocol and CDC bottle assay. It is important to check if any of the selected publications had any analysis of resistance including CDC bottle assay. If this is correct, then consider it as it could increase the amount of resistance data.

Results:

The results are coherently described with tables and figures. However, Tables 2, 3, 4, & 5 should have clear and legible descriptions.

Paragraph 2 …” From Table 2, the malaria vector was divided into three habitats …”. This sentence needs to be rephrased to make it clear. How can mosquito vectors be divided into three habitats or what do you mean? The sentence that follows this in the same paragraph should also be rephrased for clarity.
Paragraph 3 …. “The entire female Anopheles collected was morphologically identified for their species or complexes using stereomicroscopes and morphological keys” The whole of this paragraph and the next one should be combined and written clearly to convey the necessary message.
“From 15 papers reviewed, the impregnated with insecticides of DDT (4%)…” Insert the word “papers” before impregnated.
Paragraph 8 … “Table 5 shows…” Consider revising this paragraph to make it clear.

Discussion and Conclusion

The discussion highlights the different aspects of the findings on the status of insecticide resistance in different Asian countries. These are partly discussed in relation to the current literature and the status of insecticide resistance in the region. However, more discussions are required on the outcomes on the types, levels, and intensity of insecticide resistance and how multiple insecticide resistance was reported in the diversity of malaria vectors present in the region. Below are a few minor issues that need to be addressed:

Page 12, Paragraph 1: ”This became a challenge for malaria control and elimination, therefore, using the same insecticide for multiple successive IRS cycles is not recommended”. Revise this sentence and the entire paragraph to make it clear.
Page 12, paragraph 2: “…applications against resistible mosquitoes”. Which are these mosquitoes?
Page 12, paragraph 4: “This proved that pyrethroid was less effective. Meanwhile, insecticide resistance was present in malaria vectors in Asia, and the genes spread rapidly throughout the world”. This statement is misleading ..what evidence do you have that resistance genes were spreading quickly throughout the world?
Page 12, paragraph 5: It is important to state some of the 12 interventions mentioned here and their challenges and opportunities they have.

Conclusion: The conclusion is not fully drawn from the analysis of this systematic review?

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

Not applicable
Are the conclusions drawn adequately supported by the results presented in the review?

Partly

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Medical Entomology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

CITE

Report a concern

Respond or Comment

Views

22

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

https://doi.org/10.5256/f1000research.49960.r87116

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).

Based ... Continue reading

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).

Based on data extracted from 15 original articles selected from four science databases, the authors of this paper came out with a baseline review on malaria vector resistance status in Asia. This resistance concerns 23 anopheline species collected in 8 countries between 2012 and 2019, to 10 insecticides belonging to the four chemical classes mostly used for vector control. Additional information on the ecology and habitat of malaria vectors is also provided. Yet, the authors suggested some resistance management strategies, including the selection of insecticides to be used for vector control, the rotation of the interventions, and integrating vector control methods.

However, as a limitation, the low number and the content of the articles that were eligible for this study (15 papers) made it difficult to thoroughly investigate the geographic and structural distribution of insecticide resistance in target countries, as well as the underlying resistance mechanisms. It appears that the drawn conclusions are partly supported by the results of the review. Furthermore, several issues should be addressed to improve the manuscript:

1. Abstract

Line one: "remained" may be replaced by "led to"; and "due to" replaced by "which is".
Line two: The study aims to "review" the insecticide resistance status which was previously determined.
Conclusion: I would suggest replacing "complicated" with "challenging".

2. Introduction

Paragraph 1: please update the situation of malaria, according to the world malaria report 2020.
Paragraph 2: please add "partly" before "reversible", because there are many other factors that may hinder the reduction of malaria burden apart from insecticide resistance.
Paragraph 3: It is not clear which type of organism the authors are talking about in the first sentence of this paragraph. At the end of the paragraph, please change the position of "regular" and place it before "monitoring"; i.e. "regular monitoring".

3. Methods

In the last paragraph, it is said that only papers dealing with the WHO bioassay protocol were considered. Currently, the CDC bottle assay is also used for insecticide resistance testing and monitoring. Adding a separate analysis of resistance data from the CDC bottle assay, if any, could probably increase the amount of resistance data.

4. Results

Paragraph 1: A map showing the countries where insecticide resistance has been reported and the recorded resistance status for each insecticide used is missing.
Paragraph 2: Please delete "In several countries" since each species is associated with only one or two countries and not all the countries. Also, it is not clear how a malaria vector can be divided into three habitats; and also which malaria vector the authors are talking about?
Paragraph 3: Please consider revising the first sentence of this paragraph, e.g. All the female Anopheles collected were morphologically identified for their species/complexes...". The last sentence about mosquito processing is also confusing; the authors may consider revising it.
Paragraph 4: Please include "papers" before "impregnated" and replace "was" with "were".
Paragraph 5: Please delete "summarized in three resistance classes", this is confusing. The authors may just state that "bioassay results were analyzed according to WHO criteria. Also, the reference N°12 is not specific to WHO bioassay protocol, same as reference n°18; please consider revising the numbering of the references. The reference n°13 is appropriate for this paragraph.
Regarding the interpretation of the results, the authors should check, which of the WHO protocols they used. In the running WHO protocol which was deriving the revision made in 2018, the criteria for interpretation of bioassay results are different from the criteria presented in this paragraph. In the revised protocol, the resistance threshold is 90%, not 80%.
Paragraph 6: A mortality rate <97% is wide and also includes confirmed resistance, please specify the lowest mortality rates indicating possible resistance.
Paragraph 8: The first sentence may be as follows: "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..."

5: Discussion

Here are suggestions for subtitles: Types of insecticides, Insecticide resistance frequencies, Mortality rates of Anopheles populations, Interventions.
Paragraph 2: Types of insecticides - In the second sentence of the paragraph, please replace "And" with "These chemicals". Also, replace "Currently" with " Actually".
Paragraph 3: Insecticide resistance frequencies - No need to refer to tables in the discussion.
The authors may combine the first and the second sentences of this paragraph; e.g. " Resistance to various insecticides, especially to DDT and pyrethroids, was common...vector species. Multiple insecticide resistance was reported in 14 malaria vector species in Asia; these include A. stephensi...A. sinensis." For the last sentence of this paragraph and the first sentence of the next paragraph, the authors should refer to WHO guidelines for using both LLINs and IRS in specific conditions. Please consider replacing "resistible mosquitoes" with "resistant mosquitoes".
Paragraph 6: Mortality rates of the Anopheles - What is the mortality test? Is it the susceptibility test? The author should consider revising the first sentence of this paragraph. It is not clear how a test can be in a range of 98-100%, 80-97%... etc.
Paragraph 8: In the second sentence of this paragraph, the authors may replace "interventions belonging to..." with "insecticides belonging to..." and delete "durable" from the next sentence.

The following sentences should also be revised as follows:

" The accurate information about...tuns...of insecticide resistance".
"Therefore, biochemical...understand the mechanisms...in malaria vectors".
"However, several control strategies...used to overcome resistance...vector management".

6. Conclusion
The following sentences should also be revised as follows:

The reports of pyrethroid resistance were quite challenging, because..."
"integrating vector control strategies based on physical, chemical and biological methods".

7. Tables

Table 1. The title of this table may be "Article description" rather than "charactéristics".
Column 3 may be title "year of publication" rather than "publish".
Table 2: The title of this table may be "Mosquito species and their types of habitat" rather than "sample and location characteristics".
Table 4. The title of this table may be "Anopheles mortality rates in insecticide resistance bioassays" rather than "Mortality rate of insecticide resistance bioassay in Anopheles".
Table 5: The title of this table may be as follows " Insecticide resistance management strategies".

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

Not applicable
Are the conclusions drawn adequately supported by the results presented in the review?

Partly

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Medical entomology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

CITE

Report a concern

Respond or Comment

Comments on this article Comments (0)

Version 2

VERSION 2 PUBLISHED 10 Mar 2021

Open Peer Review

Reviewer Status

Reviewer Reports

	Invited Reviewers
	1	2	3
Version 2 (revision) 04 Jan 22	read		read
Version 1 10 Mar 21	read	read

Josiane Etang, Organization for Coordination of the Fight Against Endemic Diseases in Central Africa (OCEAC), Yaoundé, Cameroon; University of Douala, Douala, Cameroon
Charles M. Mbogo, Kenya Medical Research Institute-Wellcome Trust Research Program, Nairobi, Kenya
Manaswini Dehuri, orissa university of agriculture & technology, Bhubaneswar, India

Comments on this article

All Comments(0)

Add a comment

Sign up for content alerts

Browse by related subjects

Back to all reports

Reviewer Report

7 Views

28 Jan 2022 | for Version 2

Manaswini Dehuri, Department of Veterinary Parasitology, College of Veterinary Science and Animal Husbandry, orissa university of agriculture & technology, Bhubaneswar, India

7 Views Cite this report Responses(0)

Approved With Reservations

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 rewritten. In the 2nd paragraph of introduction "mainly" has been misspelt.
In methods the 6th paragraph may be rewritten for ease of understanding. Last paragraph of methods 'were' is misspelt.
In results, in the 2nd line" missing" should be deleted. 2nd paragraph of results "From Table 2" needs to be deleted. 5th line, forest "an" to be replaced with 'and'. 3rd paragraph, last line should be deleted. 4th paragraph, 2nd line needs to be re written.

Please check the manuscript thoroughly as there are many spelling and grammatical mistakes.

Statistical analysis (test of significance) ought to be done for Table 3 & 4.

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Partly
Is the statistical analysis and its interpretation appropriate?

Partly
Are the conclusions drawn adequately supported by the results presented in the review?

Yes

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Veterinary Entomology, Acarology and Protozoology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Respond to this report

Responses (0)

Back to all reports

Reviewer Report

6 Views

26 Jan 2022 | for Version 2

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

6 Views Cite this report Responses(0)

Approved

Most of the comments made on the previous version of the manuscript have been addressed. However, there is a need for further improvement of the English language through the text.

Thank you for your consideration.

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Medical entomology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

Respond to this report

Responses (0)

Back to all reports

Reviewer Report

15 Views

01 Oct 2021 | for Version 1

Charles M. Mbogo, Kenya Medical Research Institute-Wellcome Trust Research Program, Nairobi, Kenya

15 Views Cite this report Responses(0)

Approved With Reservations

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.

Introduction/Background:

The background information is sound, and the research question is easily identifiable. However, a few minor comments:

Paragraph 2 --- “The prevention of malaria mainly depends on one class of insecticides, namely pyrethroids; however, the increase in resistance to it reduces this treatment’s efficacy”. This sentence is not clear because malaria control may be done using the 4 available classes of insecticides and not the pyrethroids unless one is talking about LLINs.
Paragraph 3 –states that “Vector control is an essential aspect of a program organized to manage the disease transmitted by this type of organism”. Be specific and state what kind of organism is this.

Methods:

The methodologies applied are appropriate and adequately described. The searching process used was also appropriate. However, the authors indicated that they selected the 15 papers based on several criteria of which one included WHO bioassay protocol on the four major insecticide classes and did not consider any other bioassay protocols such as CDC bottle assay.

Currently, insecticide resistance is measured using WHO bioassay protocol and CDC bottle assay. It is important to check if any of the selected publications had any analysis of resistance including CDC bottle assay. If this is correct, then consider it as it could increase the amount of resistance data.

Results:

The results are coherently described with tables and figures. However, Tables 2, 3, 4, & 5 should have clear and legible descriptions.

Paragraph 2 …” From Table 2, the malaria vector was divided into three habitats …”. This sentence needs to be rephrased to make it clear. How can mosquito vectors be divided into three habitats or what do you mean? The sentence that follows this in the same paragraph should also be rephrased for clarity.
Paragraph 3 …. “The entire female Anopheles collected was morphologically identified for their species or complexes using stereomicroscopes and morphological keys” The whole of this paragraph and the next one should be combined and written clearly to convey the necessary message.
“From 15 papers reviewed, the impregnated with insecticides of DDT (4%)…” Insert the word “papers” before impregnated.
Paragraph 8 … “Table 5 shows…” Consider revising this paragraph to make it clear.

Discussion and Conclusion

The discussion highlights the different aspects of the findings on the status of insecticide resistance in different Asian countries. These are partly discussed in relation to the current literature and the status of insecticide resistance in the region. However, more discussions are required on the outcomes on the types, levels, and intensity of insecticide resistance and how multiple insecticide resistance was reported in the diversity of malaria vectors present in the region. Below are a few minor issues that need to be addressed:

Page 12, Paragraph 1: ”This became a challenge for malaria control and elimination, therefore, using the same insecticide for multiple successive IRS cycles is not recommended”. Revise this sentence and the entire paragraph to make it clear.
Page 12, paragraph 2: “…applications against resistible mosquitoes”. Which are these mosquitoes?
Page 12, paragraph 4: “This proved that pyrethroid was less effective. Meanwhile, insecticide resistance was present in malaria vectors in Asia, and the genes spread rapidly throughout the world”. This statement is misleading ..what evidence do you have that resistance genes were spreading quickly throughout the world?
Page 12, paragraph 5: It is important to state some of the 12 interventions mentioned here and their challenges and opportunities they have.

Conclusion: The conclusion is not fully drawn from the analysis of this systematic review?

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

Not applicable
Are the conclusions drawn adequately supported by the results presented in the review?

Partly

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Medical Entomology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Respond to this report

Responses (0)

Back to all reports

Reviewer Report

22 Views

30 Jun 2021 | for Version 1

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

22 Views Cite this report Responses(0)

Approved With Reservations

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).

Based on data extracted from 15 original articles selected from four science databases, the authors of this paper came out with a baseline review on malaria vector resistance status in Asia. This resistance concerns 23 anopheline species collected in 8 countries between 2012 and 2019, to 10 insecticides belonging to the four chemical classes mostly used for vector control. Additional information on the ecology and habitat of malaria vectors is also provided. Yet, the authors suggested some resistance management strategies, including the selection of insecticides to be used for vector control, the rotation of the interventions, and integrating vector control methods.

However, as a limitation, the low number and the content of the articles that were eligible for this study (15 papers) made it difficult to thoroughly investigate the geographic and structural distribution of insecticide resistance in target countries, as well as the underlying resistance mechanisms. It appears that the drawn conclusions are partly supported by the results of the review. Furthermore, several issues should be addressed to improve the manuscript:

1. Abstract

Line one: "remained" may be replaced by "led to"; and "due to" replaced by "which is".
Line two: The study aims to "review" the insecticide resistance status which was previously determined.
Conclusion: I would suggest replacing "complicated" with "challenging".

2. Introduction

Paragraph 1: please update the situation of malaria, according to the world malaria report 2020.
Paragraph 2: please add "partly" before "reversible", because there are many other factors that may hinder the reduction of malaria burden apart from insecticide resistance.
Paragraph 3: It is not clear which type of organism the authors are talking about in the first sentence of this paragraph. At the end of the paragraph, please change the position of "regular" and place it before "monitoring"; i.e. "regular monitoring".

3. Methods

In the last paragraph, it is said that only papers dealing with the WHO bioassay protocol were considered. Currently, the CDC bottle assay is also used for insecticide resistance testing and monitoring. Adding a separate analysis of resistance data from the CDC bottle assay, if any, could probably increase the amount of resistance data.

4. Results

Paragraph 1: A map showing the countries where insecticide resistance has been reported and the recorded resistance status for each insecticide used is missing.
Paragraph 2: Please delete "In several countries" since each species is associated with only one or two countries and not all the countries. Also, it is not clear how a malaria vector can be divided into three habitats; and also which malaria vector the authors are talking about?
Paragraph 3: Please consider revising the first sentence of this paragraph, e.g. All the female Anopheles collected were morphologically identified for their species/complexes...". The last sentence about mosquito processing is also confusing; the authors may consider revising it.
Paragraph 4: Please include "papers" before "impregnated" and replace "was" with "were".
Paragraph 5: Please delete "summarized in three resistance classes", this is confusing. The authors may just state that "bioassay results were analyzed according to WHO criteria. Also, the reference N°12 is not specific to WHO bioassay protocol, same as reference n°18; please consider revising the numbering of the references. The reference n°13 is appropriate for this paragraph.
Regarding the interpretation of the results, the authors should check, which of the WHO protocols they used. In the running WHO protocol which was deriving the revision made in 2018, the criteria for interpretation of bioassay results are different from the criteria presented in this paragraph. In the revised protocol, the resistance threshold is 90%, not 80%.
Paragraph 6: A mortality rate <97% is wide and also includes confirmed resistance, please specify the lowest mortality rates indicating possible resistance.
Paragraph 8: The first sentence may be as follows: "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..."

5: Discussion

Here are suggestions for subtitles: Types of insecticides, Insecticide resistance frequencies, Mortality rates of Anopheles populations, Interventions.
Paragraph 2: Types of insecticides - In the second sentence of the paragraph, please replace "And" with "These chemicals". Also, replace "Currently" with " Actually".
Paragraph 3: Insecticide resistance frequencies - No need to refer to tables in the discussion.
The authors may combine the first and the second sentences of this paragraph; e.g. " Resistance to various insecticides, especially to DDT and pyrethroids, was common...vector species. Multiple insecticide resistance was reported in 14 malaria vector species in Asia; these include A. stephensi...A. sinensis." For the last sentence of this paragraph and the first sentence of the next paragraph, the authors should refer to WHO guidelines for using both LLINs and IRS in specific conditions. Please consider replacing "resistible mosquitoes" with "resistant mosquitoes".
Paragraph 6: Mortality rates of the Anopheles - What is the mortality test? Is it the susceptibility test? The author should consider revising the first sentence of this paragraph. It is not clear how a test can be in a range of 98-100%, 80-97%... etc.
Paragraph 8: In the second sentence of this paragraph, the authors may replace "interventions belonging to..." with "insecticides belonging to..." and delete "durable" from the next sentence.

The following sentences should also be revised as follows:

" The accurate information about...tuns...of insecticide resistance".
"Therefore, biochemical...understand the mechanisms...in malaria vectors".
"However, several control strategies...used to overcome resistance...vector management".

6. Conclusion
The following sentences should also be revised as follows:

The reports of pyrethroid resistance were quite challenging, because..."
"integrating vector control strategies based on physical, chemical and biological methods".

7. Tables

Table 1. The title of this table may be "Article description" rather than "charactéristics".
Column 3 may be title "year of publication" rather than "publish".
Table 2: The title of this table may be "Mosquito species and their types of habitat" rather than "sample and location characteristics".
Table 4. The title of this table may be "Anopheles mortality rates in insecticide resistance bioassays" rather than "Mortality rate of insecticide resistance bioassay in Anopheles".
Table 5: The title of this table may be as follows " Insecticide resistance management strategies".

Are the rationale for, and objectives of, the Systematic Review clearly stated?

Yes
Are sufficient details of the methods and analysis provided to allow replication by others?

Yes
Is the statistical analysis and its interpretation appropriate?

Not applicable
Are the conclusions drawn adequately supported by the results presented in the review?

Partly

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Medical entomology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Respond to this report

Responses (0)

[1] 1. World Health Organization: Anopheline Species Complexes in South and South-East Asia. no. 57. 2007. Reference Source

[2] 2. World Health Organization: World malaria report 2018. Switzerland: World Health Organization, 2018. Reference Source

[3] 3. World Health Organization: Malaria Surveillance, Monitoring & Evaluation: a Reference Manual. Global Malaria Programme -WHO, 2018. Reference Source

[4] 4. Enayati A, Hemingway J: Malaria management: Past, present, and future. Annu Rev Entomol. 2010; 55: 569–591. PubMed Abstract | Publisher Full Text

[5] 5. Hemingway J, Ranson H, Magill A, et al.: Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet. 2016; 287(10029): 1785–1788. PubMed Abstract | Publisher Full Text | Free Full Text

[6] 6. Kleinschmidt I, Mnzava AP, Kafy HT, et al.: Design of a study to determine the impact of insecticide resistance on malaria vector control: A multi-country investigation. Malar J. 2015; 14: 282. PubMed Abstract | Publisher Full Text | Free Full Text

[7] 7. Kleinschmidt I, Bradley J, Knox TB, et al.: Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: a WHO-coordinated, prospective, international, observational cohort study. Lancet Infect Dis. 2018; 18(6): 640–649. PubMed Abstract | Publisher Full Text | Free Full Text

[8] 8. Mishra AK, Chand SK, Barik TK, et al.: Insecticide resistance status in Anopheles culicifacies in Madhya Pradesh, central India. J Vector Borne Dis. 2012; 49(1): 39–41. PubMed Abstract

[9] 9. Bhatt S, Weiss DJ, Cameron E, et al.: The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015; 526(7572): 207–211. PubMed Abstract | Publisher Full Text | Free Full Text

[10] 10. Kona MP, Kamaraju R, Donnelly MJ, et al.: Characterization and monitoring of deltamethrin-resistance in Anopheles culicifacies in the presence of a long-lasting insecticide-treated net intervention. Malar J. 2018; 17(1): 414. PubMed Abstract | Publisher Full Text | Free Full Text

[11] 11. PRISMA: PRISMA. [Accessed: 24-Feb-2021]. Reference Source

[12] 12. Susanna D: PRISMA 2009 check list: Current status of insecticide resistance in malaria vectors in the Asian countries: systematic review. figshare. 2021.

[13] 13. World Health Organization: Test procedures for insecticide resistance monitoring in malaria vector mosquitoes (Second edition). Second edi. Geneva, 2018. Reference Source

[14] 14. World Health Organization: Pesticides and their application, for the control of vectors and pests of public health importance, sixth edition. Department of Control of Neglected Tropical Diseases WHO Pesticide evaluation scheme (WHOPES), 2006. Reference Source

[15] 15. Susanna D: PRISMA flow diagram of systematic review inclusion and exclusion process for Current status of insecticide resistance in malaria vectors in the Asian countries. 2021; [Accessed: 24-Feb-2021]. Available: https://figshare.com/articles/figure/PRISMA_flow_diagram_of_systematic_review_inclusion_and_exclusion_process_for_Current_status_of_insecticide_resistance_in_malaria_vectors_in_the_Asian_countries_/13586078.

[16] 16. Rattanarithikul R, Harrison BA, Harbach RE, et al.: Illustrated keys to the mosquitoes of Thailand. IV. Anopheles. Southeast Asian J Trop Med Public Health. 2006; 37 Suppl 2: 1–128. PubMed Abstract

[17] 17. Sumarnrote A, Marasri N, Overgaard HJ, et al.: Status of insecticide resistance in Anopheles mosquitoes in Ubon Ratchathani province, Northeastern Thailand. Malar J. 2017; 16(1): 299. PubMed Abstract | Publisher Full Text | Free Full Text

[18] 18. Glick JI: Illustrated key to the female Anopheles of southwestern Asia and Egypt (Diptera: Culicidae). Mosq Syst. 1992; 24: 125–153. Reference Source

[19] 19. Sahu SS, Gunasekaran K, Vijayakumar T, et al.: Triple insecticide resistance in Anopheles culicifacies: A practical impediment for malaria control in Odisha state, India. Indian J Med Res. 2015; 142 Suppl(Suppl 1): S59–63. PubMed Abstract | Publisher Full Text | Free Full Text

[20] 20. Chaumeau V, Zadrozny J, Cerqueira D, et al.: Insecticide resistance in malaria vectors along the Thailand-Myanmar border. Parasit Vectors. 2017; 10(1): 165. PubMed Abstract | Publisher Full Text | Free Full Text

[21] 21. Dhiman S, Rabha B, Goswami D, et al.: Insecticide resistance and human blood meal preference of Anopheles annularis in Asom-Meghalaya border area, Northeast India. J Vector Borne Dis. 2014; 51(2): 133–136. PubMed Abstract

[22] 22. Gorouhi MA, Oshaghi MA, Vatandoost H, et al.: Biochemical Basis of Cyfluthrin and DDT Resistance in Anopheles stephensi (Diptera: Culicidae) in malarious area of Iran. J Arthropod Borne Dis. 2018; 12(3): 310–320. PubMed Abstract | Publisher Full Text | Free Full Text

[23] 23. World Health Organization: Global plan for insecticide resistance management in malaria vectors (GPIRM). France: WHO GLOBAL MALARIA PROGRAMME, 2012. Reference Source

[24] 24. Ahmad M, Buhler C, Pignatelli P, et al.: Status of insecticide resistance in high-risk malaria provinces in Afghanistan. Malar J. 2016; 15: 98. PubMed Abstract | Publisher Full Text | Free Full Text

[25] 25. Chand G, Behera P, Bang A, et al.: Status of insecticide resistance in An. culicifacies in Gadchiroli (Maharashtra) India. Pathog Glob Health. 2017; 111(7): 362–366. PubMed Abstract | Publisher Full Text | Free Full Text

[26] 26. Chareonviriyaphap T, Bangs MJ, Suwonkerd W, et al.: Review of insecticide resistance and behavioral avoidance of vectors of human diseases in Thailand. Parasit Vectors. 2013; 6: 280. PubMed Abstract | Publisher Full Text | Free Full Text

[27] 27. Vatandoost H, Hanafi-Bojd AA: Indication of pyrethroid resistance in the main malaria vector, Anopheles stephensi from Iran. Asian Pac J Trop Med. 2012; 5(9): 722–726. PubMed Abstract | Publisher Full Text

[28] 28. Marcombe S, Bobichon J, Somphong B, et al.: Insecticide resistance status of malaria vectors in Lao PDR. PLoS One. 2017; 12(4): e0175984. PubMed Abstract | Publisher Full Text | Free Full Text

[29] 29. Qin Q, Li Y, Zhong D, et al.: Insecticide resistance of Anopheles sinensis and An. vagus in Hainan Island, a malaria-endemic area of China. Parasit Vectors. 2014; 7: 92. PubMed Abstract | Publisher Full Text | Free Full Text

[30] 30. Dai Y, Huang X, Cheng P, et al.: Development of insecticide resistance in malaria vector Anopheles sinensis populations from Shandong province in China. Malar J. 2015; 14: 62. PubMed Abstract | Publisher Full Text | Free Full Text

[31] 31. Surendran SN, Jude PJ, Weerarathne TC, et al.: Variations in susceptibility to common insecticides and resistance mechanisms among morphologically identified sibling species of the malaria vector Anopheles subpictus in Sri Lanka. Parasit Vectors. 2012; 5: 34. PubMed Abstract | Publisher Full Text | Free Full Text

[32] 32. Yavaşoglu Sİ, Yaylagül EÖ, Akıner MM, et al.: Current insecticide resistance status in Anopheles sacharovi and Anopheles superpictus populations in former malaria endemic areas of Turkey. Acta Trop. 2019; 193: 148–157. PubMed Abstract | Publisher Full Text

[33] 33. Raghavendra K, Verma V, Srivastava HC, et al.: Persistence of DDT, malathion & deltamethrin resistance in anopheles culicifacies after their sequential withdrawal from indoor residual spraying in Surat district, India. Indian J Med Res. 2010; 132: 260–264. PubMed Abstract

[34] 34. Pennetier C, Bouraima A, Chandre F, et al.: Efficacy of Olyset® Plus, a New Long-Lasting Insecticidal Net Incorporating Permethrin and Piperonil-Butoxide against Multi-Resistant Malaria Vectors. PLoS One. 2013; 8(10): e75134. PubMed Abstract | Publisher Full Text | Free Full Text

[35] 35. Chareonviriyaphap T, Bangs MJ, Suwonkerd W, et al.: Review of insecticide resistance and behavioral avoidance of vectors of human diseases in Thailand. Parasit Vectors. 2013; 6: 280. PubMed Abstract | Publisher Full Text | Free Full Text

[36] 36. Ranson H, N’Guessan R, Lines J, et al.: Pyrethroid resistance in African anopheline mosquitoes: What are the implications for malaria control? Trends Parasitol. 2011; 27(2): 91–98. PubMed Abstract | Publisher Full Text

[37] 37. World Health Organization: WHO recommended insecticides for indoor residual spraying against malaria vectors. no. October, 2013; 2013. Reference Source

[38] 38. Thomsen EK, Hemingway C, South A, et al.: ResistanceSim: Development and acceptability study of a serious game to improve understanding of insecticide resistance management in vector control programmes. Malar J. 2018; 17(1): 422. PubMed Abstract | Publisher Full Text | Free Full Text

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

Abstract

Keywords

Introduction

Methods

Search strategy

Inclusion and exclusion criteria

Study selection

Data extraction and analysis

Results

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

Table 1. Article characteristics.

Table 2. Sample and location characteristics.

Table 3. WHO bioassay method.

Table 4. Mortality rate of insecticide resistance bioassay in Anopheles.

Table 5. Insecticide resistance strategies.

Discussion

Study sites

Type of insecticide

Insecticide resistance level

Mortality rate of the Anopheles

Intervention

Limitations

Conclusion

Data availability

Underlying data

Extended data

Reporting guidelines

Authors’ contributions

Acknowledgments

References

Comments on this article Comments (0)

Open Peer Review

Comments on this article Comments (0)

Open Peer Review

Reviewer Status

Reviewer Reports

Comments on this article

Browse by related subjects

Competing Interests Policy

Stay Updated