Skip to main content
Download PDF

Insecticide susceptibility status of Anopheles albimanus populations in historical malaria foci in Quintana Roo, Mexico

Malaria Journal volume 23, Article number: 165 (2024) Cite this article

Abstract

Background

Mexico has experienced a significant reduction in malaria cases over the past two decades. Certification of localities as malaria-free areas (MFAs) has been proposed as a steppingstone before elimination is achieved throughout the country. The Mexican state of Quintana Roo is a candidate for MFA certification. Monitoring the status of insecticide susceptibility of major vectors is crucial for MFA certification. This study describes the susceptibility status of Anopheles albimanus, main malaria vector, from historically important malaria foci in Quintana Roo, using both phenotypic and genotypic approaches.

Methods

Adult mosquito collections were carried out at three localities: Palmar (Municipality of Othon P. Blanco), Buenavista (Bacalar) and Puerto Morelos (Puerto Morelos). Outdoor human-landing catches were performed by pairs of trained staff from 18:00 to 22:00 during 3-night periods at each locality during the rainy season of 2022. Wild-caught female mosquitoes were exposed to diagnostic doses of deltamethrin, permethrin, malathion, pirimiphos-methyl or bendiocarb using CDC bottle bioassays. Mortality was registered at the diagnostic time and recovery was assessed 24 h after exposure. Molecular analyses targeting the Voltage-Gated Sodium Channel (vgsc) gene and acetylcholinesterase (ace-1) gene were used to screen for target site polymorphisms. An SNP analysis was carried out to identify mutations at position 995 in the vgsc gene and at position 280 in the ace-1 gene.

Results

A total of 2828 anophelines were collected. The main species identified were Anopheles albimanus (82%) and Anopheles vestitipennis (16%). Mortalities in the CDC bottle bioassay ranged from 99% to 100% for all the insecticides and mosquito species. Sequence analysis was performed on 35 An. albimanus across the three localities; of those, 25 were analysed for vgsc and 10 for ace-1 mutations. All individuals showed wild type alleles.

Conclusion

The results demonstrated that An. albimanus populations from historical malaria foci in Quintana Roo are susceptible to the main insecticides used by the Ministry of Health.

Background

Malaria is a vector-borne disease caused by Plasmodium parasites transmitted to people by Anopheles mosquitoes [1]. Robust surveillance systems, prompt diagnosis, timely treatment of parasite-confirmed cases and the use of insecticides have been the cornerstone interventions used to achieve control and to pursue malaria elimination worldwide [2]. In Latin America, malaria cases have decreased considerably during the last decade, with 0.6 million cases reported in 2021; with active transmission persisting in the Amazon basin and the Mesoamerican region with foci in Mexico, Guatemala, the “Moskitia” region between Honduras and Nicaragua, and Panama [1, 3].

As part of malaria elimination strategies, the World Health Organization (WHO) has proposed a combination of concepts and operational definitions to adapt interventions according to local settings. This framework classifies foci and transmission risk based on the characteristics of receptivity, vulnerability and transmission intensity [4]. As malaria cases decrease, countries are advised to use epidemiological data to guide intervention strategies at a fine spatial scale. Core vector control interventions such as insecticide-treated nets (ITNs) and indoor residual spraying (IRS) are recommended in areas with recent local malaria transmission (active and residual foci) and where transmission has been interrupted for more than three years but where the risk of reestablishment is present [2, 4].

In Mexico, autochthonous malaria transmission involves Plasmodium vivax (100% of cases) and occurs at foci within five states with geographic, ecological and immigration characteristics that contribute to their receptivity and vulnerability [5]. The Mexican state of Quintana Roo in the Yucatan Peninsula was a historically endemic area that has seen a dramatic reduction in cases followed by sporadic transmission limited to the municipalities of Othon P. Blanco, Bacalar, Solidaridad, and Puerto Morelos [6, 7]. In 2019, the Ministry of Health in Quintana Roo performed an epidemiological stratification and classified Bacalar and Othon P. Blanco as “cleared” foci (where cases have not been reported for at least 3 consecutive years) and Puerto Morelos as a “residual-non active” focus (with transmission not reported for at least one year), as defined by the WHO [6, 8].

Pyrethroid-based interventions together with DDT (ITNs and IRS) have been used for Anopheles vector control in Mexico since 1955 [9, 10]. The continuous use of insecticides can lead to the emergence of insecticide resistance, particularly if only one chemical group is employed [11]. In 2012, the WHO launched a global plan for managing insecticide resistance in malaria vectors [12]. A 2018 report described the occurrence of insecticide resistance in major malaria vectors from seventy-nine countries, twelve of them being in Latin America. Countries, including Guatemala and Honduras in Central America and others in South America, described the presence of phenotypic insecticide resistance in Anopheles albimanus and Anopheles darlingi, respectively [13].

Knock-down resistance (kdr) mutations in the voltage-gated sodium channel (vgsc) gene have been reported in Neotropical Anopheles [14]. Two non-synonymous mutations, L995F and L995C, have been described in An. albimanus [15, 16]. In Mexico, a previous study carried out in the Yucatan Peninsula showed the presence of An. albimanus populations resistant to DDT, deltamethrin and pirimiphos-methyl, together with elevated levels of detoxifying enzymes (glutathione S-transferases (GSTs), cytochrome P450s and esterases) [17]; however, limited data are available regarding target-site mutations in Anopheles from Mexico.

The Mexican national malaria elimination plan aims to certify MFA’s after foci characterization and effective case management and responsive vector control [5, 18]. As a part of this process, persistent transmission foci in Quintana Roo have been subjected to insecticide application with deltamethrin and bendiocarb, both with IRS, during the last 5 years to maintain low vector densities and limit the chance of local transmission [4, 6]. However, even with routine insecticide-based interventions in place, recent data on insecticide susceptibility has not been generated. This study aimed to evaluate the susceptibility status (phenotypic and genotypic) of the main Anopheles species in historical endemic foci of malaria in Quintana Roo, Mexico, as part of malaria foci characterization for malaria elimination.

Methods

Study site

The municipalities of Othón P. Blanco, Bacalar and Puerto Morelos are recognized by the Ministry of Health (MoH) as historically important malaria foci in Quintana Roo. In agreement with the MoH, the principal localities from each municipality (most populated historically endemic area with anopheline mosquitoes) were selected for this study (Fig. 1): Palmar (18°26′53.8ʺN 88°31′40.8ʺW) and Buenavista (18°52′58.9ʺN 88°14′20.3ʺW) classified as “cleared” foci, and Puerto Morelos (20°51′13.2ʺN 86°53′49.4ʺW) classified as a “residual non-active” focus from the municipalities of Othon P. Blanco, Bacalar and Puerto Morelos, respectively [4, 5, 8].

Fig. 1
figure 1

Location of the study area and localities, and general aspects of the collection sites. A Puerto Morelos-Puerto Morelos. B Buenavista-Bacalar. C Palmar-Othón P. Blanco, in Quintana Roo, Mexico

Full size image

Palmar and Buenavista are rural communities located close to the border with Belize. Puerto Morelos, considered an urban area (population = 26,921 inhabitants), is located 25 km from Cancun, one of the main tourist areas of Mexico. Activities related to agriculture and livestock are the main source of human activities in Palmar and Buenavista, and economic activities in Puerto Morelos are based on tourism and economic trade [19]. The temperature at the study sites oscillates between 25 and 29 °C during the rainy season (May–October) with an average of 1300 mm of rain per year [20]. The vegetation in the study areas is characterized by wetland forests, including swamps, mangroves and small ponds (Fig. 1) [21].

Mosquito collection and identification

Outdoor human-landing catches (HLCs) were performed by pairs of trained staff from 18:00 to 22:00 during 3-night periods at each site during October 2022 (rainy season). Collections were made within the locality, 50 m. from houses and larval habitats such as ponds and small creeks (Fig. 1). All the collected Anopheles were placed in cages (Model BugDorm-1 Insect Rearing Cage, L31 × W31 × H9 cm; Taiwan) and maintained alive between 8 and 12 h to separate those individuals that were not in optimal physiological condition to carry out bioassays. Mosquitoes were morphologically identified using keys for the Anopheles of Central America and Mexico [22].

CDC bottle bioassays

Due to the limitations of rearing an F1 generation, Anopheles spp. wild-caught adult mosquitoes were used for bioassays as reported previously [23]; each bioassay was carried out based on mosquito availability with at least 20 individuals tested per insecticide. Using the standard CDC bottle bioassay method, between 20 and 25 female mosquitoes per bottle in four replicates (Wheaton, USA) were exposed to the diagnostic doses of deltamethrin (12.5 µg/mL), permethrin (21.5 µg/mL), malathion (50 µg/mL), pirimiphos-methyl (50 µg/mL) or bendiocarb (12.5 µg/mL) and between 10 and 15 mosquitoes as control in a bottle coated with acetone [24]. When possible, replicates were carried out for both pyrethroids. For each insecticide, the number of dead/alive mosquitoes was registered at ten-minute intervals until 30 min of exposure was achieved (diagnostic time), and mortality was scored. Mosquitoes were then transferred to a separate holding container, provided sugar water, and held for 24 h to detect recovery. The percentage of dead mosquitoes at the diagnostic time was determined to characterize the susceptibility status of each population according to WHO criteria [25]. At the end of the bioassay, the mosquitoes were stored in tubes with 70% ethanol and transported to the Centre for Genetic Research of the Universidad Nacional Autónoma de Honduras and stored at − 20 °C for molecular analyses.

DNA extraction and amplification

To detect target-site mutations on genes of interest, mosquitoes exposed to pyrethroids (vgsc) and carbamates (ace-1) were chosen for analysis. Given the absence of phenotypically resistant mosquitoes, a subset of five mosquitoes exposed to deltamethrin, permethrin and bendiocarb were randomly selected per site. DNA was extracted from each specimen following the Extracta protocol (Quantabio, Beverly, Massachusetts, USA). For each specimen, hind legs were dissected and placed in a 0.2 mL conical tube with 25 μL of extraction reagent. A thirty-minute lysis at 95 °C was carried out. DNA was stabilized at a final volume of 50 μL and stored at − 20 °C until further use.

Primers designed for An. albimanus were used to amplify segments of vgsc and ace-1. The vgsc target was amplified using primers AAKDRF2 (5′—AGR TGG AAY TTY CAN GAY TTY—3′) and AADKDRR2: (5ʹ—GTT CGT CTC ATT ATC C—3ʹ) [16]. PCR reactions were carried out in a volume of 50 μL, with 25 μL of Taq Master Mix 2 × (Promega, Madison, Wisconsin, USA), 2.5 μL of each primer (10 μM), 2 μL of DNA, and nuclease-free water. The PCR programme was as follows: one cycle at 95 °C for 3 min, 40 cycles at 95 °C for 45 s, 45 °C for 45 s, 72 °C for 1 min, and 1 cycle at 72 °C for 5 min in a thermocycler (Veriti, Applied Byosistems). The ace-1 target was amplified with primers ACE1DAF: (5ʹ- TAA GAA GGT GGA CGT GTG GC -3ʹ) and ACE1DAR: (5ʹ—AGG GCA AGG TTC TGA TCG AA—3ʹ) [16]. PCR amplifications were carried out in a volume of 50 μL, with 25 μL of Taq Master Mix 2 × (Promega, Madison, Wisconsin, USA), 2.0 μL of each primer (10 μM), 2 μL of DNA, and nuclease-free water. PCR program was as follows: 1 cycle at 94 °C for 3 min, 35 cycles at 94 °C for 30 s, 61 °C for 30 s, 72 °C for 1 min, and 1 cycle at 72 °C for 10 min. PCR products were separated by electrophoresis on 1% agarose gels stained with ethidium bromide.

Sequence analysis

Amplification products of both vgsc and ace-1 were sequenced using the same primers used for PCR [16]. Purification and sequencing services were provided by Psomagen® (www.psomagen.com, Maryland, USA). The sequences were edited with the Geneious® 9.1.7 software (https://www.geneious.com); Auckland, New Zealand). SNP analyses were carried out at positions 995 and 280 for vgsc and ace-1 sequences, respectively [24]. All sequences were submitted as queries to NCBI through the BLASTn tool under default parameters to identify the most similar sequences in the GenBank nucleotide collection.

Results

Mosquito species collected

A total of 2828 anophelines were collected during the study period from the three localities. Puerto Morelos yielded the largest mosquito collections (55%) (Table 1). The most abundant species collected was An. albimanus (87% of the total mosquitoes captured), followed by Anopheles vestitipennis (10%). Additionally, specimens of Anopheles crucians (n = 64) and Anopheles gabaldoni (n = 21) both in Palmar and Buenavista, and An. darlingi (n = 1) and Anopheles neomaculipalpus (n = 1) in Palmar, were collected.

Table 1 Total Anopheles collected per locality in Quintana Roo malaria foci collected by outdoor human-landing catches during October 2022 (rainy season)
Full size table

Susceptibility assays

Bioassays were carried out for all insecticides with An. albimanus populations from Palmar and Puerto Morelos. Due to the limited number of An. albimanus collected in Buenavista, it was only possible to perform bioassays with deltamethrin. In Palmar, given the availability of specimens, additional bioassays were conducted with four insecticides (deltamethrin, bendiocarb, permethrin and malathion) with An. vestitipennis (Table 2). Anopheles albimanus populations from all three localities exhibited complete susceptibility to all insecticides, with mortalities ranging from 99 to 100% for the insecticides evaluated (Table 2, Supplemental Fig. S1). Similar results were observed for An. vestitipennis from Palmar (Table 2).

Table 2 Bottle bioassay results for malaria vectors from different sites in Quintana Roo, Mexico
Full size table

The An. albimanus population from Puerto Morelos was the only population that showed recovery to deltamethrin and permethrin at 24 h post-exposure, 2% and 2.5%, respectively.

Sequencing analysis of vgsc and ace-1 genes

Thirty-five sequences corresponding to randomly selected An. albimanus from the three localities were analysed, and one sequence per site was deposited in GenBank. Twenty-five sequences were analysed for mutations on vgsc and ten for ace-1. Five individuals exposed to deltamethrin and five exposed to permethrin from both Palmar and Puerto Morelos were included for vgsc analysis. In Buenavista, only 5 individuals exposed to deltamethrin were included for vgsc analysis. Five individuals each from Othon P. Blanco and Puerto Morelos exposed to bendiocarb were selected for ace-1 analysis. The consensus sequences from samples were aligned and compared with the reference genome from An. albimanus (KF137581) and An. gambiae (AGAP004707-RA) from GenBank and Vectorbase, respectively. An SNP analysis was carried out to identify mutations at positions 995 for vgsc and 280 for ace-1. Analysis revealed that all individuals had wild type alleles.

Discussion

According to previous reports, An. albimanus was the main malaria vector distributed across Quintana Roo, although other anopheline species like An. vestitipennis are also present and could present a risk for malaria reestablishment [25,26,27]. These results corroborate the predominance of An. albimanus as the main malaria vector species in these historical malaria foci in Quintana Roo and highlight its importance for insecticide resistance monitoring.

Malaria vectors are impacted by insecticides through vector control activities, leading to the selection of resistance in target populations [11, 14]. In addition to the use of insecticides for public health, the use of insecticides in agricultural activities constitutes an additional selection pressure [28]. The municipalities of Othon P. Blanco, Bacalar and Puerto Morelos have been areas of interest for vector control activities due to their epidemiological importance and malaria receptivity [17, 29]. These municipalities were the major areas of transmission in Quintana Roo between 2010 and 2019, where 148 out of 171 autochthonous cases at state level were reported [7, 30], and ITNs impregnated with the pyrethroid alphacypermethrin were deployed as well as IRS using bendiocarb was conducted according to local pre-elimination plans [6, 31]. Despite these interventions over the last ten years, findings here reported suggest that the local malaria vectors remain susceptible to insecticides.

A recent publication from Solis-Santoyo et al. reported An. albimanus populations that were resistant to deltamethrin and permethrin but susceptible to malathion and bendiocarb in two localities in Chiapas State in southern Mexico [32]. These results differ from the data presented here in two ways. First, the entomological collections in Chiapas were conducted in cattle corrals from localities with insecticide pressure derived from livestock and agriculture activities. Second, the diagnostic doses used in the bottle bioassays in the Chiapas study were established using a local reference strain, with insecticide concentrations lower than those recommended by globally recommended protocols [32,33,34,35]. National insecticide resistance data for malaria vectors is scarce, highlighting the importance of defining consistent methods for monitoring insecticide susceptibility of anophelines in Mexico.

Together with phenotypic data, this study provides evidence of the absence of kdr and ace-1 mutations in An. albimanus from Quintana Roo. Bioassays are key methods for detecting phenotypic resistance in vector populations, however, they can be complemented with molecular assays to detect polymorphisms that can arise at early stages of resistance development [33, 36,37,38]. Target-site screening on anophelines has been carried out routinely in other regions like Africa, yet such data are relatively scarce in Latin America [13, 39, 40]. Although a small subset of samples was screened, the approach employed aligns with similar studies in Colombia and Peru, where target-site allele screening together with bioassays has been used to improve insecticide resistance surveillance and inform insecticide resistance monitoring programs [24, 41, 42].

Current vector control guidelines highlight the importance of including a plan for insecticide resistance monitoring within national malaria elimination plans to guide decision-making for vector control interventions in different transmission scenarios and achieve MFA [4, 12]. In particular, the “Global Technical Strategy for Malaria” states that to build a robust entomological surveillance, monitoring and evaluation programme, countries should generate data in all settings, including those that are malaria-free but at risk of reestablishment, to prevent resurgence [2]. This report highlights that insecticides, including those recommended in Mexican guidelines NOM-032-SSA2-2014, can be used for immediate response in case of a malaria outbreak and as part of a preventive residual intervention programme in areas where reestablishment of transmission is a risk [43,44,45].

These findings demonstrate an absence of resistance, but it’s unclear the extent to which this can be extrapolated to other localities within the State where agricultural or public health use of insecticides may be higher. A previous study in 2007 reported the presence of pyrethroid resistance on An. albimanus populations in three localities, including Palmar (included in this study), and where enzymatic resistance mechanisms in both Quintana Roo and Campeche (also in the Yucatan Peninsula) were detected [17]. Therefore, evaluation of An. albimanus populations from other potential areas/localities where insecticide pressure exists due to routine applications should be considered.

Furthermore, future studies could include evaluations with alphacypermethrin (main pyrethroid used in recent ITN campaigns) which was not evaluated here, together with other less abundant malaria vector species, such as An. vestitipennis and An. darlingi [27, 29]. Further studies should be carried out to expand the analysis to other sites and foci in the Yucatan, such as the neighbouring state of Campeche, as well as border areas with Guatemala and Belize, including both phenotypic and genotypic approaches.

To strengthen malaria elimination in Quintana Roo and the rest of the Yucatan, routine insecticide resistance monitoring should be in place together with effective vector control coverage in highest risk areas. According to guidance provided by the WHO, each malaria-endemic country should develop a national plan where sentinel sites for routine insecticide resistance monitoring are chosen; in this context, Quintana Roo could include the data provided here as baseline information and expand upon it as needs dictate, to improve integrated vector management strategies [46].

Conclusions

Current An. albimanus populations in historical malaria foci from Quintana Roo remain susceptible to the main active ingredients in products used by the MoH for vector control in Mexico. Molecular analysis confirmed the absence of two main target-site mutations associated with resistance. This information could be used by local and national authorities to inform current vector control strategies and strengthen the malaria elimination and MFA certification process.

Disclaimer

The findings and conclusions in this paper are those of the authors and do not necessarily represent the official position of the U.S. Centers for Disease Control and Prevention.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Abbreviations

MFA:

Malaria-free area

VGSC:

Voltage-gated sodium channel

Kdr:

Knock-down resistance

WHO:

World Health Organization

CDC:

Centers for disease control and prevention

SNP:

Single nucleotide polymorphism

NCBI:

National center for biotechnology information

References

  1. WHO. World malaria report 2022. Geneva; World Health Organization 2022.

  2. WHO. Global technical strategy for malaria 2016–2030, 2021 update [Internet]. Geneva; World Health Organization 2021 [cited 2023 Feb 2]. Available from: https://www.who.int/publications-detail-redirect/9789240031357.

  3. Organización Panamericana de la Salud. Situación de la Malaria en la Región de las Américas, 2000–2016. 2016 [cited 2023 Feb 15]; Available from: https://www.paho.org/sites/default/files/2016-cha-situacion-malaria-americas.pdf.

  4. WHO. A framework for malaria elimination. Geneva; World Health Organization, 2018.

  5. Secretaría de Salud México. Plan nacional para la eliminación del paludismo 2021–2024. 2020.

  6. Servicios de Salud Quintana Roo. Plan de Eliminación del Paludismo en Quintana Roo 2018–2023. 2019.

  7. Secretaría de Salud México. gob.mx. 2023 [cited 2023 Feb 22]. Boletín Epidemiológico Sistema Nacional de Vigilancia Epidemiológica—Sistema Único de Información. Available from: http://www.gob.mx/salud/documentos/boletinepidemiologico-sistema-nacional-de-vigilancia-epidemiologica-sistema-unico-de-informacion-261547.

  8. Servicios de Salud Quintana Roo. Plan de eliminación del paludismo. Actualización 2020. 2020.

  9. van den Berg H, da Silva Bezerra HS, Chanda E, Al-Eryani S, Nagpal BN, Gasimov E, et al. Management of insecticides for use in disease vector control: a global survey. BMC Infect Dis. 2021;21:468.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Case study: Mexico—Fighting malaria without DDT. IDRC—International Development Research Centre Canada [Internet]. Ottawa, Canada: International Development Research Centre Canada; 2010 Dec [cited 2023 Dec 7]. Available from: https://idrc-crdi.ca/en/research-in-action/case-study-mexico-fighting-malaria-without-ddt.

  11. Nkya TE, Akhouayri I, Kisinza W, David JP. Impact of environment on mosquito response to pyrethroid insecticides: facts, evidences and prospects. Insect Biochem Mol Biol. 2013;43:407–16.

    Article  CAS  PubMed  Google Scholar 

  12. WHO. Global plan for insecticide resistance management in malaria vectors [Internet]. Geneva; World Health Organization, 2012. Available from: https://apps.who.int/iris/handle/10665/44846.

  13. WHO. Global report on insecticide resistance in malaria vectors: 2010–2016 [Internet]. Geneva; World Health Organization, 2018. Available from: https://apps.who.int/iris/handle/10665/272533.

  14. Silva APB, Santos JMM, Martins AJ. Mutations in the voltage-gated sodium channel gene of anophelines and their association with resistance to pyrethroids—a review. Parasit Vectors. 2014;7:450.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lol JC, Castellanos ME, Liebman KA, Lenhart A, Pennington PM, Padilla NR. Molecular evidence for historical presence of knock-down resistance in Anopheles albimanus, a key malaria vector in Latin America. Parasit Vectors. 2013;6:268.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Lol JC, Castañeda D, Mackenzie-Impoinvil L, Romero CG, Lenhart A, Padilla NR. Development of molecular assays to detect target-site mechanisms associated with insecticide resistance in malaria vectors from Latin America. Malar J. 2019;18:202.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Dzul FA, Penilla RP, Rodríguez AD. Susceptibility and insecticide resistance mechanisms in Anopheles albimanus from the southern Yucatan Peninsula, Mexico. Salud Publica Mex. 2007;49:302–11.

    Article  PubMed  Google Scholar 

  18. Santos-Luna R, Román-Pérez S, Reyes-Cabrera G, Sánchez-Arcos MR, Correa-Morales F, Pérez-Solano MA. Web geographic information system: a support tool for the study, evaluation, and monitoring of foci of malaria transmission in Mexico. Int J Environ Res Public Health. 2023;20:3282.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Data México [Internet]. [cited 2023 Jan 9]. Othón P. Blanco: Economía, empleo, equidad, calidad de vida, educación, salud y seguridad pública. Available from: https://datamexico.org/es/profile/geo/othon-p-blanco.

  20. Servicio Meteorológico Nacional de México. Resúmenes Mensuales de Temperaturas y Lluvia México 2022 [Internet]. [cited 2023 Jan 9]. Available from: https://smn.conagua.gob.mx/es/climatologia/temperaturas-y-lluvias/resumenes-mensuales-de-temperaturas-y-lluvias.

  21. Secretaría de Ecología y Medio Ambiente del Estado de Quintana Roo. Flora y Fauna Quintana Roo [Internet]. SEMA-Secretaría de Ecología y Medio Ambiente. [cited 2023 Jan 9]. Available from: https://qroo.gob.mx/sema/flora-y-fauna/.

  22. Wilkerson RC, Strickman D, Litwak TR. Illustrated key to the female anopheline mosquitoes of Central America and Mexico. J Am Mosq Control Assoc. 1990;6:7–34.

    CAS  PubMed  Google Scholar 

  23. Mackenzie-Impoinvil L, Weedall GD, Lol JC, Pinto J, Vizcaino L, Dzuris N, et al. Contrasting patterns of gene expression indicate differing pyrethroid resistance mechanisms across the range of the New World malaria vector Anopheles albimanus. PLoS ONE. 2019;30(14): e0210586.

    Article  Google Scholar 

  24. Orjuela LI, Álvarez-Diaz DA, Morales JA, Grisales N, Ahumada ML, Venegas HJ, et al. Absence of knockdown mutations in pyrethroid and DDT resistant populations of the main malaria vectors in Colombia. Malar J. 2019;18:384.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Bond JG, Moo-Llanes DA, Ortega-Morales AI, Marina CF, Casas-Martínez M, Danis-Lozano R. Diversity and potential distribution of culicids of medical importance of the Yucatan Peninsula. Mexico Salud Pública México. 2020;62:379–87.

    Article  Google Scholar 

  26. Villarreal-Treviño C, Ríos-Delgado JC, Penilla-Navarro RP, Rodríguez AD, López JH, Nettel-Cruz JA, et al. Composition and abundance of anopheline species according to habitat diversity in Mexico. Salud Pública México. 2020;12(62):388.

    Article  Google Scholar 

  27. Loyola EG, Arredondo JI, Rodríguez MH, Brown DN, Vaca-Marin MA. Anopheles vestitipennis, the probable vector of Plasmodium vivax in the Lacandon forest of Chiapas, México. Trans R Soc Trop Med Hyg. 1991;85:171–4.

    Article  CAS  PubMed  Google Scholar 

  28. Dong K. Insect sodium channels and insecticide resistance. Invertebr Neurosci IN. 2007;7:17–30.

    Article  CAS  Google Scholar 

  29. Gómez-Rivera ÁS, Chan-Chablé RJ, Canto-Mis KL, Mis-Ávila PC, Correa-Morales F, Manrique-Saide P. New distribution records of Anopheles darlingi in Quintana Roo, Southeastern Mexico. J Am Mosq Control Assoc. 2021;37:175–8.

    Article  PubMed  Google Scholar 

  30. Servicios de Salud Quintana Roo. Sistema de vigilancia epidemiológica de paludismo. 2023.

  31. Secretaría de Salud México. Manual técnico para la aplicación de rociado residual en paludismo. 2020.

  32. Solis-Santoyo F, Villarreal-Treviño C, López-Solis AD, González-Cerón L, Rodríguez-Ramos JC, Vera-Maloof FZ, et al. Resistance to pyrethroids in the malaria vector Anopheles albimanus in two important villages in the Soconusco Region of Chiapas, Mexico, 2022. Int J Environ Res Public Health. 2023;20:4258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. WHO. Test procedures for insecticide resistance monitoring in malaria vector mosquitoes [Internet]. 2nd ed. Geneva; World Health Organization, 2016. Available from: https://apps.who.int/iris/handle/10665/250677.

  34. WHO. Manual for monitoring insecticide resistance in mosquito vectors and selecting appropriate interventions [Internet]. Geneva; World Health Organization, 2022 [cited 2023 Feb 27]. Available from: https://www.who.int/publications-detail-redirect/9789240051089.

  35. Organización Panamericana de la Salud. Procedimientos para evaluar la susceptibilidad a los insecticidas de los principales mosquitos vectores de las Américas [Internet]. OPS; 2023 [cited 2023 May 19]. Available from: https://iris.paho.org/handle/10665.2/57424.

  36. WHO. Determining discriminating concentrations of insecticides for monitoring resistance in mosquitoes: report of a multi-centre laboratory study and WHO expert consultations [Internet]. Geneva; World Health Organization, 2022 [cited 2022 Dec 27]. Available from: https://www.who.int/publications-detail-redirect/9789240045200.

  37. Lissenden N, Kont M, Essandoh J, Ismail H, Churcher T, Lambert B, et al. Review and meta-analysis of the evidence for choosing between specific pyrethroids for programmatic purposes. Insects. 2021;12:826.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Owusu HF, Jančáryová D, Malone D, Müller P. Comparability between insecticide resistance bioassays for mosquito vectors: time to review current methodology? Parasit Vectors. 2015;8:357.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Antonio-Nkondjio C, Sonhafouo-Chiana N, Ngadjeu CS, Doumbe-Belisse P, Talipouo A, Djamouko-Djonkam L, et al. Review of the evolution of insecticide resistance in main malaria vectors in Cameroon from 1990 to 2017. Parasit Vectors. 2017;10:472.

    Article  PubMed  PubMed Central  Google Scholar 

  40. WHO.Malaria Threat Map [Internet]. [cited 2023 May 18]. Available from: https://apps.who.int/malaria/maps/threats/.

  41. Liebman KA, Pinto J, Valle J, Palomino M, Vizcaino L, Brogdon W, et al. Novel mutations on the ace-1 gene of the malaria vector Anopheles albimanus provide evidence for balancing selection in an area of high insecticide resistance in Peru. Malar J. 2015;14:74.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Donnelly MJ, Isaacs AT, Weetman D. Identification, validation, and application of molecular diagnostics for insecticide resistance in malaria vectors. Trends Parasitol. 2016;32:197–206.

    Article  CAS  PubMed  Google Scholar 

  43. Organización Panamericana de la Salud. Manual para la estratificación según el riesgo de malaria y la eliminación de focos de transmisión [Internet]. Pan American Health Organization; 2022 [cited 2023 Feb 14]. Available from: https://iris.paho.org/handle/10665.2/56731.

  44. WHO. Preparing for certification of malaria elimination [Internet]. Geneva; World Health Organization, 2022 [cited 2023 Feb 15]. Available from: https://apps.who.int/iris/handle/10665/364535.

  45. Sistema Integral de Normas y Evaluación de la Conformidad. SINEC. [cited 2023 Feb 14]. NOM-032-SSA2–2014. Available from: http://www.sinec.gob.mx:80/SINEC/Vista/Normalizacion/DetalleNorma.xhtml?pidn=elJqU01ldGF3RjEyY3hiaXh5a04zUT09.

  46. WHO. Framework for a national plan for monitoring and management of insecticide resistance in malaria vectors [Internet]. Geneva; World Health Organization, 2017. Available from: https://apps.who.int/iris/handle/10665/254916.

Download references

Acknowledgements

Authors would like to acknowledge the support of the team from the Unidad de Bioensayos Entomológicos and the field personnel from jurisdictions of the Ministry of Health of Quintana Roo. Thanks to Anuar Medina Barreiro and Lucrecia Vizcaino for support on administrative execution of this study.

Funding

Financial support for the development of this study was obtained from the Unidad Colaborativa para Bioensayos Entomologicos (UCBE) of the UADY, Mexico; the Center for Genetic Research of the UNAH, Honduras and the U.S. Centers for Disease Control and Prevention.

Author information

Authors and Affiliations

  1. Unidad Colaborativa de Bioensayos Entomológicos, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Mérida, Yucatán, Mexico

    Denis Escobar, Gabriela González-Olvera, Juan Navarrete-Carballo, Azael Che-Mendoza & Pablo Manrique-Saide

  2. Instituto de Investigaciones en Microbiología, Facultad de Ciencias, Universidad Nacional Autónoma de Honduras, Tegucigalpa, Honduras

    Denis Escobar

  3. Servicios Estatales de Salud de Quintana Roo, Chetumal, Quintana Roo, Mexico

    Ángel S. Gómez-Rivera, Pedro Mis-Ávila, Raquel Baack-Valle & Guillermo Escalante

  4. Centro Nacional de Programas Preventivos y Control de Enfermedades, Secretaría de Salud, Ciudad de México, Mexico

    Gerardo Reyes-Cabrera & Fabian Correa-Morales

  5. Department of Environmental Sciences, Emory University, Atlanta, GA, USA

    Gonzalo Vazquez-Prokopec

  6. Entomology Branch, Division of Parasitic Diseases and Malaria, U.S. Centers for Disease Control and Prevention, Atlanta, GA, USA

    Audrey Lenhart

Authors
  1. Denis Escobar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gabriela González-Olvera
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ángel S. Gómez-Rivera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan Navarrete-Carballo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pedro Mis-Ávila
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Raquel Baack-Valle
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Guillermo Escalante
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gerardo Reyes-Cabrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fabian Correa-Morales
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Azael Che-Mendoza
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Gonzalo Vazquez-Prokopec
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Audrey Lenhart
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Pablo Manrique-Saide
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

PMS, AL, GVP, PMA and DE conceptualized the study. GVP, AL, AZM and GGO reviewed and contributed to the protocol design. DE, ARG, JNC and GGO performed collection and biological experiments. DE carried out molecular analysis. DE and PMS drafted a first version of manuscript. All authors wrote, reviewed, read, and approved the final manuscript.

Corresponding author

Correspondence to Pablo Manrique-Saide.

Ethics declarations

Ethics approval and consent to participate.

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Escobar, D., González-Olvera, G., Gómez-Rivera, Á.S. et al. Insecticide susceptibility status of Anopheles albimanus populations in historical malaria foci in Quintana Roo, Mexico. Malar J 23, 165 (2024). https://doi.org/10.1186/s12936-024-04993-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12936-024-04993-0

Keywords

Malaria Journal

ISSN: 1475-2875

Contact us