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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.
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
Introduction
Malaria is one of the most common vector-borne diseases widespread in the tropics and subtropics 1 . 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 2019 2 . The global estimate of deaths caused by malaria reached 435,000 cases, which was the same number in 2016 3 . 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 malaria 4 .
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 dangerous 5 . 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 chemical 6 . 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 insecticides 7 .
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 countries 8 . Since 2000, malaria cases have halved due to the management and vector control interventions, estimated to have saved 660 million people 9 . 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 products 10 .
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) standard 13 . 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 procedure 14 .
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 1 15 . 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 describtion.
| Authors | Title | Year of piblication | 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 | 20 |
| 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 |
22 |
| Chareonviriyaphap
et al. |
Review of insecticide resistance and behavioral avoidance
of human diseases by vectors in Thailand |
2013 | Thailand | 2000–2010 | Parasites & Vectors | 23 |
| Chaumeau et al. | Insecticide resistance of malaria vectors along the
Thailand-Myanmar border |
2017 | Thailand | August and November 2014,
July 2015 |
Parasites & Vectors | 24 |
| 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 |
25 |
| 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 |
26 |
| 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 | 27 |
| 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 | 28 |
| Dai et al. | Development of insecticide resistance of malaria vector
Anopheles sinensis in Shandong Province In China |
2015 | China | 2003–2012 | Malaria 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 |
2012 | Sri 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 |
2019 | Turkey | April 2014 and September 2015 | ActaTropica | 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 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 |
20 |
| 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 | 22 |
| Chiang Mai-Chiang Dao, Mae Hongsom, Phrae | Thailand |
An. minimus
An. annularis |
NA | Paddy fields and
rivulet |
23 |
| 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 | 24 |
| 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 | 25 |
| Sistan and Baluchistan | Iran | An.stephensi | 733 | Coastal | 26 |
| 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 |
27 |
| Hainan Island | China |
An. sinensis,
An. vagus |
1468 | Mountainous and
ricefield |
28 |
| Shandong Province | China | An. sinensis | 4370 | Irrigated ricefield,
aquatic habitat, and small ponds |
29 |
| Batticaloa, Puttalam, Trincomalee and Ampara | Sri Lanka |
An. subpictus
An. sundaicus |
256 | Coastal and inland | 30 |
| Southeastern Anatolia and the Mediterranean | Turkey |
An. superpictus,
An. sacharovi |
1230 | Agricultural, ponds,
stream and swamps |
31 |
All the female Anopheles collected were morphologically identified for their species/complexes using stereomicroscopes and morphological keys 16 . The mosquitoes were separated by species/complexes for bioassays. The mosquitoes kept alive by giving them a sugar solution 17 .
Anopheles mosquitoes were morphologically identified at the adult stage using the Glick identification key 18 . 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 method 14 ( Table 3).
Table 3. The 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 kit 13 . The mortality rate was recorded 24 hours after exposure, while the average death was calculated for each insecticide and according to the WHO criteria 19 . Bioassy results according to the WHO citeria are susceptible (≥98% mortality), possible resistance (90–97% mortality) or confirmed resistance (<90% mortality 13 .
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.
| 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) | 20 | |||
| 45 (R) | NA | NA | NA | 92.3 (PR) | 96(PR) | 88.4 (PR) | 55 (R) | 91 (PR) | 26 | ||
| 62 (R) | NA | NA | NA | NA | 96 (PR) | 89 (PR) | 82 (PR) | 100 (S) | 25 | ||
| 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 | 31 | |
| 100 (S) | 100 (S) | 92 (PR) | NA | 100 (S) | 85 (PR) | NA | NA | NA | 20 | ||
| 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 | 22 | ||
| 81 (PR) | 95 (PR) | 100 (S) | 89 (PR) | 64 (R) | 20 | ||||||
| 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 | 23 | ||
| 100 (S) | 24 | ||||||||||
| 5 | An. minimus * | NA | NA | NA | NA | NA | NA | NA | NA | NA | 23 |
| NA | NA | NA | NA | NA | 92 (PR) | NA | NA | NA | 24 | ||
| 98-100 (S) | NA | NA | NA | 100 (S) | 100 (S) | NA | NA | NA | 27 | ||
| 6 | An. hyrcanus * | 57 (R) | NA | NA | NA | 48 (R) | 33 (R) | NA | NA | NA | 24 |
| 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 | 27 | ||
| 7 | An. barbirostris * | 69 (R) | NA | NA | NA | NA | 97-100 (PR-S) | NA | NA | NA | 17 |
| 74 (R) | NA | NA | NA | 84 (PR) | 72 (R) | NA | NA | NA | 24 | ||
| 8 | An. vagus * | 34-61 (R) | NA | NA | NA | 89-95 (PR) | 79-95 (R-PR) | NA | NA | NA | 27 |
| 67.1-88.8 (R-PR) | 77.3-88.9 (R-PR) | NA | NA | NA | NA | NA | NA | NA | 28 | ||
| 97 (PR) | NA | NA | NA | 95 (PR) | 75 (R) | NA | NA | NA | 24 | ||
| NA | NA | NA | NA | NA | 97.9-100 (S) | NA | NA | NA | 28 | ||
| 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 | 27 |
| NA | NA | NA | NA | 97 (PR) | 85 (PR) | NA | NA | NA | 24 | ||
| NA | NA | NA | NA | NA | 100 (PR) | NA | NA | NA | 27 | ||
| NA | NA | NA | NA | NA | 100 (PR) | NA | NA | NA | 17 | ||
| 10 | An. jamessi | NA | NA | NA | NA | NA | 87 (PR) | NA | NA | NA | 24 |
| 11 | An. nivipes | 0-100 (R-S) | NA | NA | NA | 90-100 (PR) | 100 (S) | NA | NA | NA | 27 |
| 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 | 27 |
| 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 | 27 |
| 14 | An. sinensis * | 30.4 (R) | 86.6 (PR) | NA | NA | NA | 35.8 (R) | NA | 32.4 (R) | NA | 29 |
| 72.7-78.4 (R) | NA | NA | NA | NA | 85.8-91(PR) | NA | NA | NA | 28 | ||
| 15 | An. subpictus * | 16-35 (R) | 49-69 (R) | NA | NA | NA | 82-96 (PR) | 72-97 (R-PR) | NA | NA | 30 |
| 16 | An. sacharovi * | 55-78.3 (R) | 58.3-90 (R-PR) | NA | 68.3-90
(R-PR) |
NA | NA | NA | NA | NA | 31 |
| 17 | An.scanloni | 84 (PR) | NA | NA | NA | NA | NA | NA | NA | NA | 24 |
| 18 | An.kochi | 82-100 (PR-S) | NA | NA | NA | 100 (S) | 100 (S) | NA | NA | NA | 27 |
| NA | NA | NA | NA | NA | 98 (S) | NA | NA | NA | 24 | ||
| 19 | An.tessellatus | 14 (R) | NA | NA | NA | 100 (S) | NA | NA | NA | NA | 27 |
| NA | NA | NA | NA | NA | 98 (S) | NA | NA | NA | 24 | ||
| 20 | An.sundaicus | 38-47 (R) | 93-98 (PR-S) | NA | NA | NA | 97-100 (S) | 100 (S) | NA | NA | 30 |
| 21 | An.aconitus | 100 (S) | NA | NA | NA | 100 (S) | 100 (S) | NA | NA | NA | 27 |
| 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 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.
| Country | Study location | habitat | 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. |
20 |
| 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, 22 |
| 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, 23, 24 |
| 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. |
25, 26 |
| 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. |
27 |
| 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. |
28, 29 |
| 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. |
30 |
| 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 |
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 conditions 24 . Also, those collected were identified for species based on their morphological characteristics 19, 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 areas 25 . 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 mosquitos 25 .
Insecticide resistance level frequencies
Resistance to various insecticide, especially to DDT and pyrethtoids, was common problem in different malaria vector species 32 . 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 LLINs 25 . 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 carbamates 33 . 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 used 33 . 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 control 3 .
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. mosquitoes 34 . 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 humans 36 . 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 months 13 . to strengthen the evidence base for the effectiveness of ongoing vector control interventions 19 . 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 Anopheles 37
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 levels 32 . 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 residues 23 .
Pyrethroids were the most commonly used insecticides for ITN and IRS, which target indoor transmission and mosquitos that bite in the room 28 . 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 world 38 . Mosquitoes have two acetylcholinesterase genes (ace-1 and ace-2), but only ace-1 was found to be significantly associated with insecticide resistance 28 . High insecticide resistance due to insensitive acetylcholinesterase (AChE) has emerged in genes spread of mosquitoes 39 . 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 resistance 40 . 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 facilities 37
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 IRS 41 . 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 LLINs 14 . WHO recommends that these insecticides' susceptibility status needs to be monitored annually 13 . However, the last two decades have seen the use of insecticides everywhere, especially pyrethroids, causing widespread resistance and compromising the effectiveness of vector control 42 . 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 resistance 32 . 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 management 26 .
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.13586078 15 .
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.13582517 12 .
Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0).
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.
Funding Statement
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.
[version 2; peer review: 1 approved
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.
References
- 1. World Health Organization: Anopheline Species Complexes in South and South-East Asia.no. 57.2007. Reference Source [Google Scholar]
- 2. World Health Organization: World malaria report 2018. Switzerland: World Health Organization,2018. Reference Source [Google Scholar]
- 3. World Health Organization: Malaria Surveillance, Monitoring & Evaluation: a Reference Manual. Global Malaria Programme -WHO,2018. Reference Source [Google Scholar]
- 4. Enayati A, Hemingway J: Malaria management: Past, present, and future. Annu Rev Entomol. 2010;55:569–591. 10.1146/annurev-ento-112408-085423 [DOI] [PubMed] [Google Scholar]
- 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. 10.1016/S0140-6736(15)00417-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 10.1186/s12936-015-0782-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 10.1016/S1473-3099(18)30172-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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] [Google Scholar]
- 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. 10.1038/nature15535 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 10.1186/s12936-018-2557-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. PRISMA: PRISMA. [Accessed: 24-Feb-2021]. Reference Source [Google Scholar]
- 12. Susanna D: PRISMA 2009 check list: Current status of insecticide resistance in malaria vectors in the Asian countries: systematic review. figshare. 2021. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. World Health Organization: Test procedures for insecticide resistance monitoring in malaria vector mosquitoes (Second edition). Second edi. Geneva,2018. Reference Source [Google Scholar]
- 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 [Google Scholar]
- 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. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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] [Google Scholar]
- 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. 10.1186/s12936-017-1948-z [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Glick JI: Illustrated key to the female Anopheles of southwestern Asia and Egypt (Diptera: Culicidae). Mosq Syst. 1992;24:125–153. Reference Source [Google Scholar]
- 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. 10.4103/0971-5916.176621 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Ahmad M, Buhler C, Pignatelli P, et al. : Status of insecticide resistance in high-risk malaria provinces in Afghanistan. Malar J. 2016;15:98. 10.1186/s12936-016-1149-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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] [Google Scholar]
- 22. 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. 10.1080/20477724.2017.1378836 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. 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. 10.1186/1756-3305-6-280 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24. Chaumeau V, Zadrozny J, Cerqueira D, et al. : Insecticide resistance in malaria vectors along the Thailand-Myanmar border. Parasit Vectors. 2017;10(1):165. 10.1186/s13071-017-2102-z [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. 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. 10.18502/jad.v12i3.82 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. 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. 10.1016/S1995-7645(12)60114-X [DOI] [PubMed] [Google Scholar]
- 27. Marcombe S, Bobichon J, Somphong B, et al. : Insecticide resistance status of malaria vectors in Lao PDR. PLoS One. 2017;12(4):e0175984. 10.1371/journal.pone.0175984 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28. 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. 10.1186/1756-3305-7-92 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29. 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. 10.1186/s12936-015-0592-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30. 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. 10.1186/1756-3305-5-34 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31. 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. 10.1016/j.actatropica.2019.02.003 [DOI] [PubMed] [Google Scholar]
- 32. World Health Organization: Global plan for insecticide resistance management in malaria vectors (GPIRM). France: WHO GLOBAL MALARIA PROGRAMME,2012. Reference Source [Google Scholar]
- 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] [Google Scholar]
- 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. 10.1371/journal.pone.0075134 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35. Okumu F: The fabric of life: what if mosquito nets were durable and widely available but insecticide-free? Malar J. 2020;19(1):260. 10.1186/s12936-020-03321-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36. Chanda E: Optimizing Strategic Insecticide Resistance Management Planning in Malaria Vectors. Insectic Resist.2016; [cited 2021 Oct 27]. 10.5772/61301 [DOI] [Google Scholar]
- 37. World Health Organization-Global Malaria Programme: WHO GLOBAL MALARIA PROGRAMME GLOBAL PLAN FOR INSECTICIDE RESISTANCE MANAGEMENT IN MALARIA VECTORS. France: WHO Library Cataloguing-in-Publication Data,2012;130. [cited 2021 Oct 17]. Reference Source [Google Scholar]
- 38. 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. 10.1016/j.pt.2010.08.004 [DOI] [PubMed] [Google Scholar]
- 39. Weill M, Malcolm C, Chandre F, et al. : The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors. Insect Mol Biol. 2004;13(1):1–7. 10.1111/j.1365-2583.2004.00452.x [DOI] [PubMed] [Google Scholar]
- 40. Kristan M, Lines J, Nuwa A, et al. : Exposure to deltamethrin affects development of Plasmodium falciparum inside wild pyrethroid resistant Anopheles gambiae s.s. mosquitoes in Uganda. Parasit Vectors. 2016;9(1):100. 10.1186/s13071-016-1384-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41. World Health Organization: WHO recommended insecticides for indoor residual spraying against malaria vectors. no. October,2013;2013. Reference Source [Google Scholar]
- 42. 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. 10.1186/s12936-018-2572-2 [DOI] [PMC free article] [PubMed] [Google Scholar]