Mosquitoes, Lymphatic Filariasis, and Public Health: A Systematic Review of Anopheles and Aedes Surveillance Strategies

Lymphatic Filariasis (LF) affects over 120 million people in 72 countries, with sub-periodic filariasis common in the Pacific. Wuchereria bancrofti has three physiological races, each with a unique microfilarial periodicity, and each race is isolated to a specific geographical region. Sub-periodic W. bancrofti is transmitted by various Aedes mosquito species, with Aedes polynesiensis and Aedes samoanus being the primary vectors in Samoa. The Aedes scutellaris and Aedes kochi groups are also important vectors in the South Pacific Islands. Anopheles species are important vectors of filariasis in rural areas of Asia and Africa. The Anopheles gambiae complex, Anopheles funestus, and the Anopheles punctulatus group are the most important vectors of W. bancrofti. These vectors exhibit indoor nocturnal biting behaviour and breed in a variety of habitats, including freshwater, saltwater, and temporary water bodies. Effective vector surveillance is central to LF control and elimination programs. However, the traditional Human Landing Collection (HLC) method, while valuable, poses ethical concerns and risks to collectors. Therefore, this review critically analyses alternative trapping tools for Aedes and Anopheles vectors in LF-endemic regions. We looked at 14 research publications that discussed W. bancrofti vector trapping methods. Pyrethrum Spray Catches (PSC), one of the seven traps studied for Anopheles LF vectors, was revealed to be the second most effective strategy after HLC, successfully catching Anopheles vectors in Nigeria, Ghana, Togo, and Burkina Faso. The PSC method has several drawbacks, such as the likelihood of overlooking exophilic mosquitoes or underestimating Anopheles populations. However, exit traps offered hope for capturing exophilic mosquitoes. Anopheles populations could also be sampled using the Anopheles Gravid Trap (AGT). In contrast, the effectiveness of the Double Net Traps (DNT) and the CDC Light Trap (CDC LT) varied. Gravid mosquito traps like the OviArt Gravid Trap (AGT) were shown to be useful tools for identifying endophilic and exophilic vectors during the exploration of novel collection techniques. The Stealth trap (ST) was suggested for sampling Anopheles mosquitoes, although specimen damage may make it difficult to identify the species. Although it needs more confirmation, the Ifakara Tent Trap C design (ITT-C) showed potential for outdoor mosquito sampling in Tanzania. Furvela tent traps successfully captured a variety of Anopheles species and are appropriate for use in a variety of eco-epidemiological settings. By contrast, for Aedes LF vectors, no specific sampling tool was identified for Aedes niveus, necessitating further research and development. However, traps like the Duplex cone trap, Resting Bucket Trap (RB), and Sticky Resting Bucket trap (SRB) proved effective for sampling Aedes albopictus, offering potential alternatives to HLC. This review emphasises the value of looking into alternative trapping methods for Aedes and Anopheles vectors in the LF-endemic region. Further research is required to determine the efficacy of novel collection techniques in various contexts, even if PSC and AGT show promise for sampling Anopheles vectors. The identified traps, along with ongoing research, provide valuable contributions to vector surveillance efforts in LF-endemic regions, enabling LF control and elimination strategies to advance.


Introduction
The elimination of Lymphatic Filariasis (LF) and malaria, two mosquito-borne diseases, is planned for 2030 through preventive chemotherapy and vector control measures [1,2].Sensitive, quick, and species-specific diagnostic methods for parasite detection in humans and vectors are required to confirm the cessation of transmission, and they are crucial for determining disease prevalence [3][4][5][6][7][8].These technologies define intervention endpoints and confirm the efficacy of mass drug administration (MDA) programmes [9].
Medical entomologists have been utilizing molecular xenomonitoring (Mx) for decades to assess the risk of transmission of vector-borne illnesses (VBDs) by detecting human infections in arthropod vectors.Mx, a powerful tool for tracking disease transmission, as it can detect microfilarial DNA in mosquito samples even in trace amounts, served as a proxy for human infection surveillance related to VBDs [10][11][12][13][14][15][16][17].Creating xenomonitoring systems for programmatic use that are accurate, reliable, and cost-effective can be challenging due to the diverse vector-parasite combinations.
In 2022, the World Health Organization (WHO) estimated that there were 120 million people infected with W. bancrofti and 12 million people infected with Brugia malayi.The disease is most common in tropical and subtropical regions, and it is estimated that 80% of all cases are found in Africa (World Health Organization, Global Programme to Eliminate Lymphatic Filariasis.Progress Report 2022.Geneva: World Health Organization; 2023).Research on mosquito sampling techniques for Anopheles and Aedes vectors of diurnally sub-periodic (DspWB) and nocturnally periodic (NpWb) W. bancrofti (Wb) is lacking, despite the abundance of literature emphasizing the use of Mx for LF elimination with a Culex quinquefasciatus (C.q.)-W.bancrofti (Wb) vector-parasite combination.Choosing the best Mx tool for public health programmes and surveillance is critical, even though Anopheles and Aedes vectors are less responsible for the LF burden than Culex-transmitted filariasis.
The epidemiological significance of parasite DNA prevalence in local vector mosquitoes can be demonstrated by improving mosquito sampling techniques for local mosquito vector species.This will lead to sufficient sample sizes and more accurate prevalence estimates.Consequently, these enhancements have increased the operational value of LF and malaria elimination programmes.
The utilisation of different mosquito sampling techniques by vector control programmes in diverse eco-epidemiological settings may lead to biased assessments of species diversity and abundance.This systematic review critically examines the prevalence, geographic distribution, and bio-ecology of sub-periodic filariasis, specifically focusing on Anopheles spp.and Aedes spp.The review also investigates and compares the effectiveness of various Mx traps.The primary objective is to identify the most suitable Mx tool for various tasks, considering the available information on sampling techniques while taking into account the biology of the mosquito species acting as vectors.

Prevalence and Distribution of Lymphatic Filariasis
Over 120 million people in 72 countries across Asia, Africa, the Western Pacific, and parts of the Caribbean and South America are affected by LF.Sub-periodic filariasis caused by W. bancrofti is particularly prevalent in the Pacific region, including the islands of Tahiti, Samoa [18], Tonga, and Fiji, Australia, New Guinea, and the nearby Melanesia, Micronesia, and Polynesia islands are all part of the Pacific region [19].
The South Pacific islands exhibit a similar pattern of patchy filariasis distribution as the rest of the world [20,21].Early data from Fiji [22] revealed a low frequency of 6.4% among residents of the Labasa, compared to a high prevalence of 25.2% in Taveuni.The prevalence rates in various communities appeared to be influenced by the behaviours of the population and the proximity of densely populated vector areas to human settlements, increasing the likelihood of infection transmission.Particularly in the Nancowry group of islands, Nicobar district, the day-biting Aedes (Downsiomyia) niveus transmit the diurnally sub-periodic W. bancrofti disease in India [23][24][25][26][27][28].

Physiological Races of W. bancrofti
There are three physiological races of W. bancrofti, each having a unique microfilarial periodicity.Apart from the Polynesian sub-region, the nocturnally periodic race is widely distributed in tropical and sub-tropical environments worldwide.A nocturnally sub-periodic race is found in the jungle regions of West Thailand, while the diurnally sub-periodic race is isolated to the Polynesian sub-region [29][30][31].Each race has unique intermediate hosts, and the microfilarial periodicity of each race coincides with the biting rhythm of the principal vector mosquitoes.The Aedes (Finlaya) poecilus type is responsible for transmitting nocturnally periodic W. bancrofti in the Phillipines.Additionally, the Aedes (Finlaya) kochi group serves as efficient vectors for the diurnally sub-periodic race in the Polynesian region.

4.
The Aedes (Ochlerotatus) vigilax type is the primary vector of the diurnally sub-periodic race of W. bancrofti endemic in the New Caledonian region.

5.
Aedes (Stegomyia) polynesiensis-type mosquitoes are the principal vectors of the diurnally sub-periodic form W. bancrofti in the Polynesian region.
In the South Pacific Islands, the sub-periodic W. bancrofti is primarily transmitted by A. pseudoscutellaris, and along with A. polynesiensis, they were efficient transmitters, and the night-biting A. fijiensis of the kochi group was equally efficient [22,39,40].C. quinquefasciatus, the vector of periodic W. bancrofti, could also transmit sub-periodic W. bancrofti to a limited extent in the Society Islands and Fiji [22,40].Further studies by Burnett [41], Rossen [42], and Symes [22,40] confirmed these findings, emphasizing the need for re-examination potential vectors, particularly in areas where members of the A. scutellaris and kochi groups have been reported [43].
In India's Andaman and Nicobar Islands, DspWb is transmitted by the day-biting Aedes (Downsiomyia) niveus, a tree-hole breeder, with diurnal biting behaviour.A. polynesiensis in American Samoa and Western Samoa exhibits similar biting behaviour, primarily diurnal with a small proportion biting at night [27,44].Sampling A. niveus presents a significant challenge for researchers and LF control programmes conducting surveillance [45].
In Samoa, efficient vectors of sub-periodic W. bancrofti include A. polynesiensis, A. upolensis, and in the Tongo region A. tabu. A. polynesiensis prefers resting in dry coconut husks, tree holes, the undersides of partially detached bark on dead trees, and similar sheltered sites.A. upolensis is a true forest dweller, diurnally active and breeds in tree hollows or cavities of dead trees.A. tabu is predominantly found in plantations but also occurs in shady areas in villages, limited to the Tonga islands.Their breeding habitats include tree holes, artificial containers, coconut shells, and leaf axils of taro [35] Other important Aedes vectors are A. poecilus, the A. scutellaris group, and O. togoi (earlier known as A. togoi) [46].

The Anopheles Vector and Its Ecology
Anopheles species are significant vectors of malaria and filariasis in rural regions of Asia and Africa.Some examples include the A. punctulatus group in Papua New Guinea (PNG) [47], A. gambiae s.s., A. arabiensis, and A. funestus on the Kenyan coast [48]; A. subpictus in the Indonesian islands of Flores and Timor [49]; and A. gambiae s.s. in Ghana [50], which transmits both P. falciparum and W. bancrofti parasites.
There are about 26 Anopheles species vectoring Bancroftian and B. filariasis.Of these, eighteen species transmit W. bancrofti, three species transmit B. malayi, and five species transmit both parasites.A. barbirostris is the only known vector of B. timori.Among them, the A. funestus group and members of the A. gambiae complex including A. gambiae s.s., A. arabiensis, A. melas, and A. merus are the most important vectors of W. bancrofti.A. merus breeds in saltwater, while the other three species breed in freshwater [49] with A. melas often associated with mangroves [51].
In Africa, the A. gambiae complex and A. funestus are the most important vectors of W. bancrofti [52].These vectors exhibit indoor nocturnal biting behaviour.A. gambiae is highly anthropophilic and employs a "patrolling" or "ranging" flight strategy to encounter host cues.A. funestus is highly endophilic and anthropophilic but can display moderate to high zoophagy in areas with large livestock populations.They breed throughout the year, with A. funestus preferring permanent water bodies and certain stagnant water bodies, while the A. gambiae complex breeds in temporary or man-made water bodies like pools, puddles, brick pits, fields, construction sites, hoof prints, or tire tracks.This adaptability allows them to maintain population numbers even during dry months, promoting year-round malaria transmission [53].
In Asia, W. bancrofti is transmitted by A. jeyporiensis candidiensis and A. minimus in China, by A. flavirostris in the Philippines, and by A. balabacensis, A. maculatus, A. letifer, and A. whartoni in Malaysia [49].The A. punctulatus group includes A. punctulatus, A. farauti, and A. koliensis, which are the principal vectors of the periodic W. bancrofti in Papua New Guinea (PNG), West Papua (Indonesia), Solomon Islands, and Vanuatu [54,55].
The A. punctulatus group prefers to breed in small, shallow, exposed pools devoid of other flora and fauna [56].In an inland village in PNG, 99.9% of A. punctulatus were recorded.A. farauti is a coastal species that can breed in brackish water but is also found at altitudes over 1000 m above sea level in PNG. A. koliensis is a nocturnal mosquito with a preference for indoor feeding and breeds in streams at the forest margins.In East Sepik Province, PNG, both A. punctulatus and A. koliensis were found to be potential vectors. A. punctulatus breeds along river edges during the rainy season and, during the dry season, along sections of the dried-up river, forming numerous sun-lit puddles that serve as additional breeding sites [57].Aedes and Anopheles species which are responsible for transmitting W. bancrofti in various regions of the world is listed below (Table 1)

Methodology 2.1. Database Search and Systematic Review
We systematically analysed published research articles using specific databases including Google Scholar, ResearchGate, PubMed, and ScienceDirect.Our search focused on topics such as molecular xenomonitoring, W. bancrofti (Wb), Lymphatic Filariasis, Mosquito sampling methods, mosquito trapping techniques, Aedesand Anopheles-transmitted filariasis, and sub-periodic filariasis.Through this search, we identified 41 relevant articles.
In our analysis, we specifically examined the efficiency of different mosquito trapping techniques, with a focus on sampling Aedes and Anopheles mosquito vectors of W. bancrofti.This information is crucial for conducting molecular xenomonitoring, VBD surveillance, and implementing effective public health programmes.After careful evaluation, we selected 14 records that met our inclusion criteria, making them eligible for data collection and comprehensive analysis.

Exclusion Criteria
Brugian filariasis studies involved the Anopheles species in transmission.LF was transmitted by Culex mosquitoes.
Studies focused on human blood surveys for microfilarial infection detection for Transmission Assessment Surveys (TAS).

2.
Co-endemicity of LF and malaria transmitted by the Anopheles vector.
Mosquito trapping techniques employed in diverse LF-endemic regions for Transmission Assessment Surveys 5.
Efficiency assessment of various mosquito traps.
The flow chart below depicts the search strategies for sampling techniques related to Anophelesand Aedes-mediated W. bancrofti.Full-text records meeting the inclusion criteria were selected for review.The study design was described using all five steps of the PRISMA (Preferred Reporting Items for Systematic Reviews) (Figure 1) checklist to ensure review quality.The flow chart below depicts the search strategies for sampling techniques related to Anopheles-and Aedes-mediated W. bancrofti.Full-text records meeting the inclusion criteria were selected for review.The study design was described using all five steps of the PRISMA (Preferred Reporting Items for Systematic Reviews) (Figure 1) checklist to ensure review quality.

Sampling Strategies for LF-Endemic Aedes and Anopheles Vectors
The 14 included publications focused on assessing trapping techniques for Aedes and Anopheles vectors transmitting W. bancrofti in endemic regions where an Mx of LF has been conducted.While the HLC method has been essential, ethical concerns and risks to collectors necessitate exploring alternative trapping tools [51].
This review critically analysed the efficiency of seven traps for sampling Anopheles LF vectors such as PSC, GT, BGS, CDC LT, ET, DNT, and AGT (Table 2) and discussed novel collection methods including the Stealth trap, Ifakara Tent Trap, Mbita trap, Furvela tent trap as alternatives to HLC [51].For Aedes LF vectors, four different traps were analysed (BGS, GT, CDC LT, DNT) along with the Resting Bucket Trap (RB), Sticky Resting Bucket trap (SRB), Duplex cone trap, and novel sticky trap [51].PSC was the second most efficient method after HLC, effectively capturing Anopheles vectors in Nigeria, Ghana, Togo, and Burkina Faso [7,51,69,79].However, PSC has drawbacks, as it may miss exophilic mosquitoes or underestimate Anopheles populations [72,78,80,81].The Exit trap was useful for trapping exophilic mosquitoes [71].BGS showed varying results in different settings, being more effective in some regions but less so in others [17,34,50].The AGT appeared to be an appropriate trap for sampling Anopheles populations [51].CDC LT and DNT also had variable efficiency [71].In Mali, HLC was observed to be more productive than the PSC [82].
The review identifies traps with potential for xenomonitoring LF vectors, but further studies are needed to assess their effectiveness in different settings [51,73].The CDC Light Trap captured more Culex and fewer Anopheles vectors [51].A comparison of various vector sampling techniques in Anophelesand Aedes-mediated LF-endemic regions is provided in Table 3.

Methods for Sampling Mosquitoes to Conduct Disease Surveillance and Research
It is critical to comprehend the behaviour, distribution, and function of mosquitoes as disease vectors in order to effectively combat illnesses such as LF, malaria, dengue, Zika, and others.Scientists are able to advance disease management by gaining insights into mosquito populations and their interactions with the environment through the use of a variety of collection techniques.

Human Landing Catch (HLC):
Employing mosquitoes' biological propensity to seek a blood meal for reproduction, this technique captures mosquitoes as they descend onto human or animal hosts.They are captured using an oral aspirator prior to biting the host [83].
Pyrethrum Spray Collection (PSC): PSC entails the application of an insecticide aerosol containing pyrethrum within confined spaces.Mosquitoes are rendered immobile and disoriented, causing them to descend onto a white cloth, from which they can be collected [84].
CDC Light Trap: These devices attract and capture adult mosquitoes using artificial light sources.By simulating natural light sources, the trap attracts mosquitoes for further study [85].
CDC Gravid Trap: Specialized equipment built to capture female mosquitoes in search of sites where they can lay their eggs.These devices leverage the inherent behaviour of mosquitoes by employing attractants such as organic matter to establish an optimal environment for oviposition [86].
Biogents Sentinel (BGS) Trap: These traps imitate human or animal hosts by combining chemical attractants, visual signals, and heat.The chemical lures and design of the trap increase its attraction to blood-seeking mosquitoes [86].
Window Exit Trap: As mosquitoes enter or leave designated areas, this trapping system captures them.It is comprised of two chambers, one of which is baited with heat and carbon dioxide to simulate human presence and entice mosquitoes to enter; these mosquitoes are then collected in the exit chamber [87].
DNT: This consists of two box nets, one protecting the collector and a second larger net, which is placed directly over the inner net.The outer net is raised off the ground so that mosquitoes attracted to the human bait are collected between the two nets [88].

Novel Tools for Sampling Anopheles Vectors: W. bancrofti and P. falciparum Transmission
Gravid mosquito traps, such as the OviArt Gravid Trap (AGT), offer valuable sampling tools for both endophilic and exophilic vectors, enhancing the detection of parasite-infected mosquitoes for VBD surveillance and Transmission Assessment Surveys.AGT, specifically targeting gravid Anopheles mosquitoes, has shown promising results with improved catch size compared to other traps like the Box gravid trap.However, further improvements in battery protection and transportation convenience are needed.AGT is made of a rectangular basin measuring 45 cm × 33 cm × 11.5 cm (length × width × height), with a 4 cm hole on the side and a 6 L rectangular basin.An open plastic tube (collection chamber) was inserted into the hole and the other opening of the tube was sealed with fibreglass netting to prevent trapped mosquitoes from escaping.The tube was placed and secured halfway into an aluminium collapsible pipe.The flexible tube was connected to a 12 V fan that provided suction on the water surface [89].
The Stealth trap (ST) has been recommended as a valuable tool for capturing Anopheles mosquitoes, particularly A. gambiae s.l., in West Africa.While ST shows high capture rates, it may cause damage to specimens, making species identification challenging [82].The Ifakara Tent Trap C design (ITT-C) has been considered promising for outdoor mosquito sampling in Tanzania and has been evaluated for routine malaria vector surveillance.Modifications and validation in different settings are needed for optimal performance [90].The ITT has been reported to be comparatively superior in terms of capture rates compared to HLC [91] and CDC LT [92].However, operators' exposure to mosquito bites necessitates modifications for improved performance [93].
Furvela tent traps provide an efficient way to capture Anopheles mosquitoes, especially in situations with diverse mosquito fauna.Combining CDC-LT or window-exit traps (to sample endophagic mosquitoes) with Furvela tent traps (to sample exophagic ones) allows robust sampling of diverse mosquito species [94].Both CDC-LT and Furvela tent traps are portable and suitable for surveillance.These tools hold promise for effective vector monitoring in various eco-epidemiological settings [82, 90,94,95].

Aedes Mosquito Sampling Techniques: W. bancrofti Transmission
In a typical endemic setting for DspWb mediated by A. niveus, BGS, DNT, GT, and HLC were deployed for vector mosquito sampling to assess vector infection.However, none of these trapping methods were suitable for sampling A. niveus, with BGS and DNT capturing more A. albopictus and A. aegypti, and GT capturing C. quinquefasciatus [61].Thus, there is currently no specific sampling tool identified for A. niveus apart from HLC.
In contrast, BGS was found to sample adequate numbers of A. polynesiensis and A. samoanus vectors of LF in Samoa.However, the sampling method suitable for A. polynesiensis in Samoa may not be applicable for A. niveus in Nancowry Islands, and BGS showed limited efficiency in capturing A. niveus [16].For A. albopictus, some traps like the Duplex cone trap, Resting Bucket Trap (RB), and Sticky Resting Bucket (SRB) have been reported to be efficient in sampling.
The Duplex cone trap was found to be the most productive trap for sampling A. albopictus, offering a promising alternative to HLC [96].RB and SRB traps were also effective in capturing A. albopictus in various habitats, with SRB showing higher capture rates [97].Additionally, the novel sticky trap was reported to be more precise than the ovitrap for sampling A. albopictus in urban settings [98].
These findings suggest that, for specific mosquito species like A. niveus, further research and development of the suitable sampling tools are needed.Meanwhile, traps like the Duplex cone trap, RB, SRB, and novel sticky trap show promise for efficient sampling of A. albopictus.

Conclusions
In conclusion, this review has focused on the assessment of trapping techniques for Aedes and Anopheles vectors responsible for transmitting W. bancrofti in LF regions endemic to LF.While the Human Landing Collection (HLC) method has been instrumental, it raises ethical concerns and poses risks to collectors, underscoring the need for alternative trapping methods.Among the traps examined, the Pyrethrum Spray Catches (PSC) method demonstrated high efficiency in capturing Anopheles vectors across multiple countries.However, it may not effectively capture exophilic mosquitoes and could underestimate Anopheles populations.Other traps like the Anopheles Gravid Trap (AGT) and the Exit Trap, also showed potential, although their effectiveness varied in different settings.
In the case of Aedes vectors, traps like BGS and CDC LT proved useful in specific regions, yet no dedicated sampling tool was identified for A. niveus apart from HLC. Novel traps like the Stealth trap, the Ifakara Tent Trap C design (ITT-C), and Furvela tent traps offer promising alternatives for capturing Anopheles mosquitoes in diverse eco-epidemiological settings.Regarding A. albopictus, traps like the Duplex cone trap, Resting Bucket Trap (RB), and Sticky Resting Bucket (SRB) exhibited high efficiency in various habitats.Nonetheless, further research is imperative to develop suitable sampling tools for specific mosquito species like A. niveus.In summary, these findings provide valuable insights into efficient sampling strategies for LF-endemic Aedes and Anopheles vectors, thereby facilitating vector surveillance and enhancing disease control efforts.

Figure 1 .Figure 1 .
Figure 1.Identification of Sampling techniques for Anopheles-and Aedes-mediated W. bancrofti through databases.PRISMA flow diagram of study selection and inclusion.3. Sampling Strategies for LF-Endemic Aedes and Anopheles Vectors Figure 1.Identification of Sampling techniques for Anophelesand Aedes-mediated W. bancrofti through databases.PRISMA flow diagram of study selection and inclusion.
1.1.2.Types of W. bancrofti Infection Identified, Based on Their Ecological Distribution 1.The Culex fatigans type, transmitted by the Culex pipiens complex, including races like Culex fatigans, is known as Culex quinquefasciatus and Culex molestus.This is the most widely distributed ecological type [29].2. The Anopheles type, in tropical Africa, Anopheles gambiae, Anopheles funestus, and related species are the principal vectors of W. bancrofti in rural areas, while other regions have vectors such as Anopheles maculatus, Anopheles whartoni, Anopheles flavirostris, and Anopheles punctulatus [29].3.

Table 2 .
Studies carried out in different LF-endemic regions where the principal vectors are Aedes and Anopheles.

Table 3 .
Applicability of different vector sampling techniques to sample Anopheles and Aedes vectors in LF-endemic regions apart from the Human Landing Collection.