Knockdown Resistance (kdr) Associated Organochlorine Resistance in Mosquito-Borne Diseases (Anopheles albimanus, Anopheles darlingi, Anopheles dirus and Anopheles punctipennis): A Systematic Review Study

doi:10.21203/rs.3.rs-5012727/v1

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Knockdown Resistance (kdr) Associated Organochlorine Resistance in Mosquito-Borne Diseases (Anopheles albimanus, Anopheles darlingi, Anopheles dirus and Anopheles punctipennis): A Systematic Review Study

https://doi.org/10.21203/rs.3.rs-5012727/v1

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Introduction:

Anopheles albimanus, Anopheles darlingi, Anopheles dirus, and Anopheles punctipennis are malaria vectors in many world regions. The resistance of these vectors against insecticides, especially organochlorine insecticides, has significantly hindered efforts to control them. Although one of the causes of resistance is kdr mutation, studies in this field have been done sporadically. As a result, this study was conducted to investigate the kdr mutation in the mentioned vectors using a systematic review method.

Methods

This study was conducted as a systematic review of kdr mutation in Anopheles albimanus, Anopheles darlingi, Anopheles dirus, and Anopheles punctipennis. Therefore, the international scientific databases PubMed, Web of Science, Cochrane Library, Scopus, Science Direct, and Google Scholar were searched, and all relevant articles were extracted and surveyed without a time limit until the end of June 2024. The quality assessment of the articles was done using the Strobe checklist.

Result

Five articles were included in the systematic review process. The findings indicated that kdr mutation was not observed in any of the four species of Anopheles albimanus, Anopheles darlingi, Anopheles dirus, and Anopheles punctipennis, and the causes of resistance are other factors, including other metabolic resistances such as MFO and NSE.

Conclusion

Based on the findings, kdr mutation does not play any role in creating resistance in Anopheles albimanus, Anopheles darlingi, Anopheles dirus, and Anopheles punctipennis. Considering these vectors' various behavioral and biological characteristics, other metabolic and behavioral can cause resistance against organochlorine insecticides. Consequently, there is a need to conduct studies on the factors that cause resistance in these vectors.

Anopheles albimanus

Anopheles darlingi

Anopheles dirus

Anopheles punctipennis

Knockdown resistance

Organochlorine insecticide

Anopheles is the primary vector of malaria in the world and has more than 400 species, 40 of which are known as malaria vectors. Anopheles albimanus is one of the main malaria vectors in the Caribbean islands, Central America, and the northern regions of South America (1). An. albimanus is zoophilic, exophagic, and corpuscular and has higher compatibility than other anopheline species (2). This species has a flexible behavior that can affect its spread in lower and more temperate latitudes (3). Various insecticides, such as organochlorine, organophosphorus, and pyrethroids, have been used to control this vector. However, in recent decades, this vector's resistance against the insecticides DDT, lambda-cyhalothrin, deltamethrin, and malathion has been widely reported (4–6). Various factors have been mentioned as the causes of resistance in this vector, but the most important of them is metabolic resistance, especially knockdown resistance (kdr), which has been considered in the field of resistance to organochlorine insecticides. Although studies have mentioned various results in this field, further investigation is required (7).

Anopheles darling is one of the main vectors of malaria, and as the dominant species in the Neotropical region, it leads to malaria transmission (8). This vector is widely present in South and Central America, Panama, Mexico, Argentina, and the Atlantic coast (8, 9). The population of Anopheles darlingi increased due to deforestation and human settlements (10, 11). This species is the focal vector of malaria in South and Central America, causing an increase in malaria in this region (12, 13). Due to its endophilic properties, this transporter is controlled by the IRS. After the use of DDT to fight Anopheles was suspended, organochlorine, organophosphorus, and pyrethroids, including lambda-cyhalothrin and deltamethrin, are used to fight this vector (14). However, recently, the resistance of this vector against insecticides has increased and even led to cross-resistance between insecticides. The existence of cross-resistance among different insecticides, which can be caused by mutations in target sites and metabolic mechanisms, is a serious obstacle to its use in malaria control programs (15).

Anopheles dirus is another malaria vector in Southeast Asia and is common in Thailand, Myanmar, Indochina, and China (16–18). It has seven different types; the most common types are A, B, C, and D. These species have high biological, behavioral, and biological diversity and remarkable ability to adapt to the environment (16, 19, 20). This vector is prevalent in dense forest areas and is one of the leading causes of falciparum malaria in this region. Behavioral change and their ability to adapt to the environment have increased the resistance of this vector against various types of insecticides (21).

The development of resistance in Anopheles mosquitoes has made it very difficult to control these vectors. Mechanisms of resistance to insecticides in Anopheles include metabolic resistance, resistance at the target site, cuticular resistance, and behavioral resistance, of which resistance at the target site and metabolic resistance play a significant role in creating resistance to insecticides (22). Resistance at the target site, with a change in the amino acid sequence of the voltage-gated sodium channel, leads to a decrease in the sensitivity of mosquitoes to pyrethroid and organochlorine insecticides and is known as kdr (23, 24). The widespread distribution of insecticide resistance, especially organochlorine insecticides worldwide, has affected the epidemiology of malaria. Therefore, raising awareness about the impact of insecticides and the potential for resistance is crucial for understanding and managing malaria transmission. Accordingly, monitoring the resistance of malaria vectors against insecticides to implement control programs is essential to verify the effectiveness of control tools. Thus, this study was conducted to investigate the presence of kdr mutation in causing resistance to organochlorine insecticides in An. albimanus, An. darlingi, and An. dirus worldwide using a systematic review method.

Study protocol

This study is a systematic review in the field of kdr mutation in An. albimanus, An. darlingi, An. dirus, and An. punctipennis based on PRISMA guidelines (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) (25). Also, this study has been registered in the International Prospective Register of Systematic Reviews (PROSPERO) with the code CRD42021231605.

Search strategy

Articles were extracted without a time limit until the end of June 2024 from PubMed, Web of Science, Cochrane Library, Scopus, Science Direct, and Google Scholar databases and keywords of resistance, knockdown mutations, knockdown resistance, kdr, insecticide resistance, organochlorine insecticide, organochlorine, insecticide, dichloroethane, DDT, aldrin, lindane, dieldrin, malaria vectors, Anopheles, An. albimanus, An. darlingi, An. dirus, and An. punctipennis were searched in the title, abstract and keywords in singular and compound form using AND and OR operators.

Inclusion and exclusion criteria

All the English-language articles published worldwide that were conducted on malaria vectors, including An. albimanus, An. darlingi, An. dirus, An. punctipennis, and kdr resistance and mutation were investigated, and resistance to organochlorine insecticides was evaluated in them. High-quality articles were included in the study. Articles that did not meet the inclusion criteria investigated other insecticides, or were conducted using case reports or case series were excluded from the study.

Quality assessment

The quality assessment of the articles was done based on 22 parts of the STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) checklist, examining compliance with the principles of writing and implementation in the title, method of reporting findings, limitations, and conclusions. Each item on the checklist is assigned a score based on importance, with a maximum possible score of 33 (26).

Screening and data extraction

At first, considering the inclusion and exclusion criteria, the title and abstract of the articles were examined independently by two researchers. Two researchers then reviewed the full text of the articles. If an article was rejected, the reason was documented. In cases of disagreement between the two researchers, a third reviewer evaluated the article. Data extraction was done using a previously prepared checklist, including study location, study time, insecticide type, vector type, and kdr mutation.

Study selection

Globally, about 40 species of Anopheles mosquitoes carry malaria. Understanding their biological and behavioral characteristics, as well as effective control methods, is essential for combating and reducing malaria. However, insecticide resistance poses a significant obstacle to controlling these vectors. Organochlorine insecticides have been used to control these vectors for a long time, but resistance, especially of the kdr type, has limited the use of these insecticides.

Four species of An. albimanus, An. darlingi, An. dirus, and An. punctipennis, have caused the spread of malaria in different regions worldwide. The cause of resistance in these vectors has not been widely investigated in the world, and it is unclear whether kdr mutation is the cause of resistance in these vectors. In the following section, kdr mutation was investigated in the mentioned transporters.

Kdr in Anopheles albimanus

An. albimanus is one of the main malaria vectors in various world regions (3). In the past, resistance to organochlorine insecticides, which are widely used to deal with this vector, has been reported. Studies of metabolic mechanisms or insensitivity of the target site, such as mutations in the sodium channel gene (VGSC), have mentioned the cause of this resistance (27, 28). It has been shown that increasing the activity level of esterases and oxidases plays an important role in creating resistance in this vector (29). High oxidase activity and a target site mechanism have also been implicated in cross-resistance between DDT and pyrethroids in An. albimanus (30). Considering the research done on kdr mutation in An. albimanus, only one study has been conducted in Colombia by Orjuela et al. (2019). in which sequencing of all the samples in the forward and reverse direction has been done in the context of three codons of 1010, 1013, and 1014, which are related to resistance to organochlorine insecticides and pyrethroids in malaria vectors. The findings identified the GTT codon at position 1010 (V1010), AAC codon (for asparagine) at position 1013 (N1013), and TTA and TTG codons (for leucine) at position 1014, revealing that no amino acid mutation was observed in the sequences and there is no kdr mutation in them (31). Even though this study has shown that the kdr mutation plays a role in An. Albimanus resistance, it is not resistant to organochlorine insecticides, and more studies are required to confirm this claim.

Kdr in Anopheles darlingi

An. darlingi is one of the vectors of malaria in the world, and it can be found especially in the Amazon region and Africa. This vector has a wide global occurrence and differentiation in genetic, morphological, and behavioral traits, leading to the creation and spread of various insecticide resistance mechanisms (32, 33). For many years, neurotoxic insecticides have been used to deal with this vector. To deal with this vector, it is necessary to evaluate its sensitivity; however, the resistance or sensitivity of this vector has rarely been evaluated so far. Organochlorine insecticides, especially DDT, cause paralysis or death of this transporter by targeting the voltage-gated sodium channel (27, 34). However, kdr mutation has recently been considered. In the study of Orjuela et al. (2019) in Colombia done on An. darlingi, knockdown mutations did not create resistance to organoleptic insecticides. In this study, all samples were analyzed in the forward and reverse direction of sequencing, and three codons, 1010, 1013, and 1014, are related to resistance to organochlorine insecticides and pyrethroids in malaria vectors. The findings identified the GTT codon at position 1010 (V1010), AAC codon (for asparagine) at position 1013 (N1013), and TTA and TTG codons (for leucine) at position 1014, indicating that no amino acid mutation was observed in the sequences and there is no kdr in them (31). Fonseca-González et al. (2009) in Colombia investigated kdr in An. darlingi against organochlorine insecticides and pyrethroids. The findings showed that all populations of An. darlingi were sensitive to deltamethrin, permethrin, and malathion. Resistance to lambda-cyhalothrin and DDT was observed in the population, demonstrating 65 to 75% mortality. Cross-resistance between these two insecticides was also observed. However, specific resistance due to kdr was not observed, and the cause of resistance was reported to be increased metabolism through MFO and NSE (6). Based on the investigated studies, it can be mentioned that kdr mutation has not been observed in An. darlingi, and the cause of resistance in this vector can be metabolic mechanisms and increased activity of oxidases and esterases.

Kdr in Anopheles dirus

An. dirus complex is one of the malaria vectors that can be found in Asia, especially its forest areas. This species has biological and ecological differences and behavioral changes when it is in contact with humans and exposed to environmental stimuli which can improve carrying capacity and environmental adaptation (16, 35, 36). These changes can increase resistance to control measures in this vector. Organochlorine insecticides have been one of the main insecticides used to combat this vector since a long time ago, and the main cause of resistance to these insecticides was reported to be kdr mutation (37). Verhaeghen et al. (2009) investigated kdr in 73 An. dirus mosquitoes in Vietnam. Based on their study, sequencing was performed in the DIIS6 region of the para-type sodium channel gene for the samples to identify kdr, but the results did not show any kdr mutations among the samples (38). Sumarnrote et al. (2017) investigated the kdr mutation in An. dirus against the insecticide deltamethrin in Vietnam. The results of the genetic sequencing of the samples did not show any L1014F or L1014S substitutions in the VGSC gene.

Additionally, the attenuation ratio of this transporter against deltamethrin was 100%, which indicates that it is sensitive to this insecticide (39). In the study by Zeng et al. (2017) in Hainan Province, the attenuation ratio of An. dirus against the insecticides deltamethrin (0.05%), DDT (4%), malathion (5%), and cyfluthrin (0.15%) was 100%, revealing the high sensitivity of this vector against organochlorine insecticides. It should also be mentioned that no kdr mutation was observed in this study (21). In general, kdr mutation has not been detected to create resistance in this vector, and this vector has a high sensitivity to insecticides, including organochlorines.

Kdr in Anopheles Punctipennis

An. punctipennis is a common and widespread malaria vector in the United States and North America (3). This vector can transmit Plasmodium vivax and Plasmodium falciparum [9]. It can also transmit Plasmodium odocoilei to wild animals such as deer, which increases their biodiversity and makes fighting it more complex (40, 41). Also, creating resistance to insecticides in this vector can be another limitation of controlling it. While searching, only one study was found which investigated the kdr mutation in this vector. Orjuela et al. (2019) investigated the kdr mutation in An. punctipennis. The results of sequencing the samples identified the GTT codon at position 1010 (V1010), AAC codon at position 1013 (N1013), and TTA and TTG codons at position 1014. which shows that no amino acid and kdr mutations were observed in the sequences (31). Although this study has shown no kdr mutation in this vector, more studies are needed to confirm this issue.

In this study, kdr resistance in An. Albimanus was investigated, and the findings showed no kdr resistance mutation in this vector. There are various mechanisms for Anopheles’ insecticide resistance, including behavioral, cuticular, metabolic, and target site resistance, in which metabolic resistance and resistance to the target site play a greater role in creating resistance to insecticides (42). In the studies that were conducted, it was mentioned that metabolic resistance creates resistance in An. Albimanus. In sodium channel 9, natural mutations at positions N1013 (S), V1010 (L), I1048 (N), L1014 (F/S/C/W), N1575 (Y) and S1156 (G) are found to be associated with the phenotype resistance in Anopheles (6, 43). Besides, only mutations identified at position 1014 are involved in reducing sodium channel sensitivity to insecticides (7, 44). An. Albimanus mutations at positions L1014F and L1014C can lead to kdr, which has not been identified in the studies carried out so far (30). However, it should also be noted that only a small region of the VGSC gene is often evaluated in sequencing. As a result, there is a possibility that mutations and resistance created by mutations occurring in different regions of the gene can be communicated, so it is recommended to examine a longer region of the gene (7). In general, the studies reporting kdr mutation's role in creating resistance in An. Albimanus have not been provided. However, confirmation of this issue requires conducting more studies in this field.

In the present systematic review, kdr resistance in An. darlingi and An. dirus was not reported. Other studies have shown that in the populations of An. darlingi and An. dirus, metabolic mechanisms have played an essential role in resistance, and the level of functional oxidases has increased in resistant Anopheles (6). Additionally, in pyrethroid-resistant Anopheles, an increase in the levels of non-specific esterases has been reported (43). In vectors resistant to organochlorine insecticides and pyrethroids, metabolic detoxification and reduction of cuticular penetration have also been observed (45–49). These cases can generally cause high resistance levels without kdr mutations (50). Other studies investigating the resistance of Anopheles An. darlingi has reported high levels of AChE against organophosphates and carbamates (29). In a study conducted in Mexico, an increase in the level of cytochrome P450 and the activity of glutathione S-transferase and esterase was observed in DDT-resistant Anopheles (29). Studies have shown that in the population of An. darlingi, resistance to carbamates and organophosphates is associated with mutations in ace-1, resistance to pyrethroids is associated with mutations in the VGSC gene, and resistance to deltamethrin and alpha-cypermethrin is associated with cytochrome P450 CYP9K1 and overexpression of CYP6P5 (30, 51, 52).

Considering the presence of kdr mutations in most DDT-resistant Anopheles species in different regions of the world, the absence of this mutation in the mentioned vectors can reflect genetic limitations or reduce insecticide pressure (51, 53). Also, the activity of An. dirus is strongly related to the foothills, deep forests, and forest margins, which can affect its behavioral characteristics and reduce the effect of insecticides on them (16). Since no kdr mutation was observed in the mentioned vectors, metabolic and behavioral resistance mechanisms can play a major role in developing resistance. Hence, we can mention different factors and mechanisms that create resistance in An. darlingi and An. dirus. Overall, the studies have not implicated the kdr mechanism in developing resistance. However, studies in this field are few, and more studies are needed.

Based on the findings, kdr mutation does not play any role in creating resistance in An. albimanus, An. darlingi, An. dirus, and An. punctipennis. Considering these vectors various behavioral and biological characteristics, other metabolic and behavioral causes can play a role in creating resistance against organochlorine insecticides. Besides, limited studies have been done to investigate the resistance of kdr in these transporters; as a result, it is necessary to conduct more studies on the activity of these transporters in the field of resistance-causing factors.

Ethics approval and consent to participate

Not applicable.

Availability of data and materials

All data obtained from this study are included in the text of article.

Competing interests

The authors declare no competing interests.

Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Authors contributions

EA determined the title, wrote and registered the protocol, and submitted the article. EA and SD extracted the files from the databases. EA and SD, screening, and selection of final reports. EA, data extraction. EA wrote the article. All authors read and approved the final manuscript.

Acknowledgments

The authors thank the Research Vice-chancellor of Shiraz University of Medical Sciences.

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Table 1. Characteristics of the articles included in the systematic review

Author	Year Study	Place Study	Sample Size	Type of *Anopheles*
Orjuela L (31)	2019	Colombia	126	An. albimanus, An. Darling and An. Punctipennis
Fonseca-González I (6)	2009	Colombia	120	An. darlingi
Verhaeghen K (38)	2009	Mekong region	60	An. dirus
Sumarnrote A (39)	2017	Thailand	34	An. dirus
Zeng LH (21)	2011	China	90	An. dirus

No competing interests reported.

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Knockdown Resistance (kdr) Associated Organochlorine Resistance in Mosquito-Borne Diseases (Anopheles albimanus, Anopheles darlingi, Anopheles dirus and Anopheles punctipennis): A Systematic Review Study

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