Searching for the proverbial needle in a haystack: advances in mosquito-borne arbovirus surveillance

Searching for the proverbial needle in a haystack: advances in mosquito-borne arbovirus surveillance Surveillance is critical for the prevention and control of mosquito-borne arboviruses. Detection of elevated or emergent virus activity serves as a warning system to implement appropriate actions to reduce outbreaks. Traditionally, surveillance of arboviruses has relied on the detection of specific antibodies in sentinel animals and/or detection of viruses in pools of mosquitoes collected using a variety of sampling methods. These methods, although immensely useful, have limitations, including the need for a cold chain for sample transport, cross- reactivity between related viruses in serological assays, the requirement for specialized equipment or infrastructure, and overall expense. Advances have recently been made on developing new strategies for arbovirus surveillance. These strategies include sugar-based surveillance, whereby mosquitoes are collected in purpose-built traps and allowed to expectorate on nucleic acid preservation cards which are submitted for virus detection. New diagnostic approaches, such as next-generation sequencing, have the potential to expand the genetic information obtained from samples and aid in virus discovery. Here, we review the advancement of arbovirus surveillance systems over the past decade. Some of the novel approaches presented here have already been validated and are currently being integrated into surveillance programs. Other strategies are still at the experimental stage, and their feasibility in the field is yet to be evaluated. Keywords: Arboviruses, Surveillance, Mosquito, Sentinel animals, Honey-based surveillance, Next-generation sequencing Background Africa [4] and Brazil [5] have highlighted the continuing Arthropod-borne viruses (arboviruses) transmitted by threat emerging and re-emerging arboviruses pose. mosquitoes are of public health and veterinary import- With the exception of YFV [6] and JEV [7], there are ance globally causing disease syndromes including en- currently few vaccines or antiviral drugs available against cephalitis, viral haemorrhagic disease and arthritis. most of these viruses. Thus, prevention and control of Dengue viruses (DENVs) alone cause an estimated 96 most arboviruses is almost solely reliant on effective million clinical cases a year, especially in the tropics and mosquito management. This can be enhanced by sur- sub-tropics [1]. The flaviviruses, Japanese encephalitis veillance, where detection of elevated or emergent virus virus (JEV) and West Nile virus (WNV), are major activity serves as a warning system to implement appro- causes of viral encephalitis throughout their geograph- priate actions to reduce the severity and duration of out- ical range. Recently, the expansion of chikungunya breaks. However, designing an appropriate arbovirus (CHIKV) [2] and Zika (ZIKV) [3] viruses in the Western surveillance system is challenging. Arboviruses have Hemisphere, and the yellow fever (YFV) outbreaks in complex transmission cycles with dual-host tropism: they replicate in vertebrate hosts (such as birds or mammals) and arthropod hematophagous vectors (such as mosqui- toes or ticks) [8]. This complexity needs to be accounted * Correspondence: ana.ramirez1@my.jcu.edu.au for, and an ideal surveillance system should rely on differ- College of Public Health, Medical and Veterinary Sciences, James Cook University, PO Box 6811, Cairns, QLD 4870, Australia ent sources of information (Fig. 1), and can include Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. Ramírez et al. Parasites & Vectors (2018) 11:320 Page 2 of 12 Fig. 1 Transmission cycles of arboviruses and different strategies for arbovirus surveillance meteorological data, evidence of virus infection in verte- for WNV [14]. In Argentina [15] and Brazil [16], dead brate hosts, entomological surveys, virus detection in vec- howler monkeys acted as an early warning for sylvatic tors, and reports of human or animal disease. The scale of transmission of YFV and prompted vaccination cam- surveillance can vary regionally [9] and is particularly paigns in the human population in 2008 and 2017, challenging in remote locations, or in areas with limited respectively. resources and infrastructure. A major limitation of monitoring human and animal Given the broadness of this subject, few attempts have cases is that confirmatory laboratory testing is not avail- been made to provide a synthesis of arbovirus surveil- able in many limited resource countries, so arboviral dis- lance methods. The objective of this review is to de- ease is diagnosed on clinical symptoms. However, scribe the development and implementation of symptoms can overlap between arboviruses, as well as mosquito-borne arbovirus surveillance strategies. First, with non-arbovirus pathogens, complicating their clin- we evaluate traditional methods that have been com- ical diagnosis. Furthermore, most arbovirus infections monly used where arboviruses are a public health threat, are mild, or sub-clinical, which may lead to them being then outline and assess recently developed methodolo- under-reported. Ultimately, using human and animal gies, before identifying future research needs. case data is not ideal, since it indicates that active trans- mission is already occurring. Methods for arbovirus surveillance Monitoring human and animal disease Vertebrate host arbovirus surveillance: sentinel animals Human or animal case surveillance relies on hospitals, Sentinel animals provide evidence of virus activity and laboratories and health practitioners notifying public increased risk to the target animal or human population health authorities of confirmed or suspected cases of [17]. For this, immunologically naïve animals are de- arbovirus infection that occur in the population. Almost ployed in a specific location, bled on a defined schedule, every state in the United States conducts surveillance of and tested for the presence of virus-specific antibodies human WNV cases as a part of the national arbovirus as an indication of exposure. Virus isolation or molecu- surveillance system, ArboNET [10], whilst in Australia, lar detection on pre-seroconversion blood samples can human arbovirus disease notifications are monitored provide an isolate and/or a sequence for genotypic ana- using the National Notifiable Disease Surveillance Sys- lysis of circulating virus strains [18]. A suitable sentinel tem (NNDSS) [11]. These surveillance systems require animal should: (i) be susceptible to the monitored virus; strict case definitions and laboratory diagnostic testing (ii) develop an antibody response that can be detected in criteria, as well as demographic, clinical, laboratory and serological assays; (iii) have low morbidity and mortality; epidemiological information [12]. In the summer and (iv) be attractive to the vector; (v) be easy to handle; and autumn of 1999, reports of dead crows played a critical (vi) allow for multiple sampling [12]. role in identifying the outbreak of WNV in New York Different vertebrate species are used as sentinels [13]. With bird cases often preceding human cases by up (Table 1) and choice of animal is dependent on the tar- to 3 months, it served as an ideal early warning system get virus. In terms of WNV surveillance, some studies Ramírez et al. Parasites & Vectors (2018) 11:320 Page 3 of 12 Table 1 Animal species that have been used as sentinels for arbovirus surveillance Animal Virus Example location References Chickens WNV USA, UK [119, 120] SLEV USA [121] MVEV, WNV Australia [122] KUN Pheasants WNV, SLEV, EEEV USA [123, 124] Pigs JEV Japan, Australia, Thailand [125–127] Dogs WNV USA, Africa [128, 129] JEV Japan, Thailand [130, 131] Sheep and goats RVFV Africa, Saudi Arabia [132–134] Cattle BTV, Akabane Australia, Papua New Guinea, Japan [135–137] Horses EEEV, WEEV Argentina [138] WNV, SLE Colombia [139] Hamsters EEEV, VEEV USA, Central and South America [140–143] Non-human primates YFV Brazil, Argentina [144–147] Abbreviations: WNV, West Nile virus; SLEV, St. Louis encephalitis virus; MVEV, Murray Valley encephalitis virus; WNV , West Nile virus (Kunjin subtype); EEEV, KUN eastern equine encephalitis virus; JEV, Japanese encephalitis virus; RVFV, Rift Valley fever virus; BTV, bluetongue virus; WEEV, western equine encephalitis virus; VEEV, Venezuelan equine encephalitis virus; YFV, yellow fever virus have suggested that the use of sentinel chickens is the are mobile, it is difficult to determine exactly when and most sensitive indicator of virus activity, when compared where an animal acquired the infection, especially since with other methods, such as detection of seroconversion IgG antibodies are present for the life of the animal. in wild birds and virus isolation from mosquito pools [19]. Whilst they can undoubtedly serve as an early Mosquito-based arbovirus surveillance warning system, in some areas of the USA, sentinel Mosquito-based arbovirus surveillance monitors vector chickens to monitor WNV have proven unsuccessful, populations and virus infection prevalence within them. since seroconversions were detected only after the onset Mosquitoes are collected, identified, pooled by species of human cases [20, 21]. or other taxonomic grouping, and sent to the laboratory Even though sentinel animal surveillance enables the where they are tested for virus infection status. There timely detection of circulating arboviruses, it also comes are different strategies for mosquito collection. In areas with limitations. In many cases, the locations of enzootic with low-level mosquito infections or early in the trans- arbovirus foci are unknown or difficult to access. Thus, mission season, efforts should be directed towards per- animals are placed near towns, which may be too far forming targeted surveillance at “hotspots” where a high from virus foci to detect elevated activity [22]. Further- likelihood of arbovirus presence is suspected; as vector more, some animals serve as amplifying hosts (i.e. pigs populations increase later in the season, the number of for JEV) increasing the risk of transmission to humans sampling sites should be expanded for broader monitor- [23]. Additionally, the cost of rearing and replacing sen- ing [29]. There are a variety of commercial traps de- tinel animals, especially in remote locations, can be pro- signed to collect mosquitoes, the design of which and hibitive [24, 25], and bleeding large animals presents a application have been comprehensively reviewed else- workplace health and safety hazard [26]. There are also where [30, 31]. It is essential that the selection of the ethical considerations associated with the use of sentinel collection method takes into consideration the physio- animals [27]. Finally, closely related viruses (i.e. JEV, logical and behavioural characteristics of the studied WNV and Murray Valley encephalitis virus (MVEV)) vector [32] (Table 2). can cross-react in some serological assays, requiring A variety of methods have been utilized for detection confirmation by other methods to obtain unequivocal of arboviruses in captured mosquitoes. Historically, results [28]. arbovirus isolations were conducted in animals, such as Another approach to vertebrate host surveillance relies suckling mice and chickens. With the development and on monitoring wild vertebrates or livestock, which are establishment of cell lines, virus isolation in cell culture captured, sampled and released [12]. However, one of became the gold standard for arbovirus detection from the biggest issues with surveillance of these animals is pools of mosquitoes. This method can only detect viable the cross-reaction between antibodies and the interpret- viruses, so a cold chain keeping samples at ultralow tem- ation of the results. Given that many of these animals peratures during transport needs to be maintained to Ramírez et al. Parasites & Vectors (2018) 11:320 Page 4 of 12 Table 2 Collection methods commonly used for mosquito-based arbovirus surveillance Mosquito Collection method Advantages Disadvantages References behaviour Host seeking Human-landing catches Larger collections than resting or oviposition Most traps require batteries or AC power to [148] collections. Collections can be increased by operate. Depending on environmental BG Sentinel [149] using CO or chemical lures conditions, the fan components are prone to malfunction. Require CO as the primary CDC-light trap 2 [150] attractant EVS-trap [151] Mosquito Magnet™ [152] Animal baited traps [153–155] Resting CDC-backpack aspirator More blood fed mosquitoes collected, ideal Labour intensive and inefficient mosquito [156] for blood meal analysis capture Prokopack [157] Resting boxes [158–160] Oviposition Sticky ovitraps Mosquitoes have bloodfed and thus a higher Smaller collections than other methods, thus [161–163] probability of detecting positive mosquitoes. all mosquitoes can be easily processed Gravid Aedes trap (GAT) [66] Targets Aedes-borne viruses such as DENV and CHIKV CDC-gravid trap [164] Although this method has been used for arbovirus studies in the past, it has considerable drawbacks, including the risk of infection to the collector, which is considered unethical even illegal in some countries Abbreviations: CDC, Centers for Disease Control and Prevention; EVS, Encephalitis virus surveillance preserve virus infectivity [33]. Maintenance of a cold arbovirus of human (and veterinary) importance, with chain requires the use of dry ice or liquid nitrogen ship- some even available in multiplex format [41]. In spite of pers in the field, which can be logistically challenging. this, it is important to note that RT-PCR and qRT-PCR Virus isolation is time consuming and obtaining defini- will only pick up RNA from viruses that the primers and tive results can take weeks, which defeats the purpose of probes were designed to detect [42]. Historically, one of using it for early warning. Some viruses do not replicate the main drawbacks of this method has been its high in- on common cell lines used in the laboratory. This can stallation and reagent costs, limiting its use in be the case for previously unrecognized or unknown vi- low-resource settings. However, recently, costs associ- ruses, such as insect-specific flaviviruses (ISF) that do ated with qRT-PCR have dropped considerably making not grow in vertebrate cells [34]. Virus isolation can be it an accessible alternative for routine screening. expensive and requires special infrastructure and trained Rapid antigen detection assays were initially developed personnel. However, even with these limitations, virus to test clinical samples but have proven to be a useful isolation is still an important method for arbovirus diag- tool to test mosquito pools in the field [43]. These assays nostics, as it increases viral titer, which allows for full allow for qualitative detection of arboviruses, and have genome sequencing and provides viruses for phenotypic the advantage of being rapid, without the need for spe- characterization. cialized equipment. Currently, there are tests commer- Nucleic acid detection using RT-PCR has become one cially available for a variety of viruses including CHIKV of the most popular methods of virus detection and has [44], DENV [45] and WNV [43], among others. In potentially displaced virus isolation as the new gold Singapore [46] and Malaysia [47], a dengue NS1 rapid standard. Real time quantitative RT-PCR (qRT-PCR) test has been used to detect infected mosquitoes as part platforms, such as TaqMan®, are ideal for routine testing of a routine surveillance programme. These tests have of mosquitoes, since they reduce processing time signifi- shown high specificity for the target virus, although cantly (sometimes to less than an hour), allowing for some assays have reduced sensitivity when compared high throughput screening [35, 36]. Since these assays with molecular methods [48, 49]. However, although detect both infectious virus and RNA, they have com- they may provide an underestimate of infection rate, parable or better sensitivity than virus isolation [37]. De- they provide a first screen and have applicability in re- pending on the protocol or application, these techniques gions without access to more resource intensive or ex- enable the detection of one infected individual from a pensive diagnostic capacity. pool of up to 5000 non-infected mosquitoes [38, 39]. Traditional mosquito-based surveillance systems that Additionally, although a cold chain is still recommended, target processing of pools of mosquitoes come with in- it has been possible to detect viral RNA from dead mos- herent limitations. Mosquito populations often have very quitoes kept for several weeks in hot and humid condi- low carriage rates, whereby only one in 1000 mosquitoes tions by qRT-PCR [33, 39, 40]. Currently, a variety of is actually infected [50]. To increase the probability of qRT-PCR assays exist for the detection of almost every detection, large numbers of mosquitoes are required, Ramírez et al. Parasites & Vectors (2018) 11:320 Page 5 of 12 resulting in numerous mosquitoes to identify, pool and Free-standing sugar bait stations have the potential to test, increasing laboratory costs and turnaround time. be used instead of CO -baited traps [59]. These stations Additionally, many traps require attractants, such as consist of a dental wick soaked in sucrose solution and a CO , to increase collections. This comes in the form of floral lure, such as phenyl acetaldehyde. Mosquitoes dry ice or pressurized cylinders, which may not be read- lured to the station feed on the wick, which is tested for ily available, or only allow overnight deployment of the expectorated viral RNA. The sugar bait stations do not trap. A cold chain of storage at < -50 °C is required to require CO or electricity, so a number of stations can preserve the integrity of the virus for detection, which be deployed simultaneously, thus increasing geographical can be a challenge in remote locations. Finally, special- coverage. In a proof of concept, the sugar bait stations ized laboratory equipment and infrastructure is required detected WNV before sentinel animals seroconverted in for diagnostics, which might not be available in develop- California. However, this method appears more effica- ing countries. cious in arid habitats, probably because of lack of com- petition with other sucrose sources, such as floral nectars. As sugar bait stations facilitate increased geo- Novel methods for arbovirus surveillance graphical coverage, they may have higher costs associ- The majority of mosquito species feed on carbohydrates ated with analysing an increased number of samples, (i.e. flower nectar, honeydew or rotting fruit) which are although this would be offset by savings by not having to the primary energy source of their diet [51]. One excep- use CO baited light traps. tion is Ae. aegypti, which appears to obtain enough en- Sugar-based surveillance has several advantages over ergy from blood and rarely feeds on sugar in domestic traditional methods. When mosquito populations are el- environments [52]. The ingestion of carbohydrates is im- evated, sorting becomes time consuming, and a high portant for the survival of the mosquito, and plays an in- number of pools can overwhelm laboratory capacity. direct role in disease transmission, allowing an infected When combined, these issues can reduce the ability to female to live long enough to become infective [53]. It provide results in a timely manner. Sugar-based methods was hypothesized by Doggett et al. [54] and confirmed potentially overcome these issues, since only 1-2 FTA® by van den Hurk et al. [55], that infected mosquitoes ex- cards per trap are tested, compared to a variable number pectorate virus while sugar feeding, which can be de- of mosquito pools. As only transmitting mosquitoes will tected using molecular assays. This finding led to the yield positive results, the presence of virus in saliva ex- development of novel sugar-based approaches for the pectorate is a better estimate of transmission risk. FTA® detection of arboviruses in mosquitoes in the field. This cards can preserve viral RNA for up to 28 days [56], system integrates purpose-built CO -baited box traps, making this an ideal alternative for surveillance in re- which house nucleic acid preservation cards (Flinders mote or difficult to access locations, where regular ser- Technology Associates, FTA® cards) soaked in honey vicing of traps is not feasible. Results suggest that and on which mosquitoes feed and expectorate onto sugar-based surveillance is a more sensitive indicator of [56]. The FTA® cards inactivate any expectorated viruses arbovirus activity than sentinel animals. In northern and preserve the liberated RNA. The cards are then sent Australia, it has been possible to detect WNV before KUN to the laboratory in the post without requirement of a sentinel animal seroconversions [60]. However, a com- cold-chain, where they are screened for viruses using parison of the sugar-based surveillance system with molecular assays. existing strategies still needs to be thoroughly evaluated. Commonly used traps employed to collect mosquitoes Sugar-based surveillance, using either SMACK or EVS (i.e. CDC-light trap and Encephalitis Virus Surveillance, traps, has been successfully incorporated into existing EVS, trap) require batteries to operate which can be lo- surveillance programs in Australia, with multiple detec- gistically challenging. To circumvent this limitation, a tions of MVEV, WNV , RRV, BFV, Edge Hill virus KUNV non-powered CO -baited passive box trap (PBT) was de- and Stratford virus [61–64]. veloped by Ritchie et al. [57] to collect and house mos- Honey-soaked FTA® cards have the potential to be in- quitoes. A variation of the PBT, the sentinel mosquito tegrated into surveillance of Ae. aegypti-borne arbovi- arbovirus capture kit (SMACK) was developed to in- ruses. The cards have been used in Biogents sentinel crease mosquito survivorship and consequently increase traps (BGS traps) and modified double sticky ovitraps the probability of infected mosquitoes feeding on the for the detection of CHIKV in French Guiana [65]. The FTA® card [58]. Although designed for weekly or fort- approach appeared time consuming with only one nightly servicing, the SMACK has demonstrated similar CHIKV positive FTA® card out of 234 analysed. Traps trap efficacy to the CDC-light trap and EVS trap in over- that are more efficient at collecting Ae. aegypti may be night collections, making it an alternative to traps that able to increase trap collections, thus increasing the like- require batteries to operate. lihood of detecting virus. For instance, the Gravid Aedes Ramírez et al. Parasites & Vectors (2018) 11:320 Page 6 of 12 Trap (GAT) [66] collects 2.4 times more Ae. aegypti and systems would require modification of current trap de- significantly more gravid females than double sticky ovi- signs to selectively capture mosquito excreta. traps [67], which could increase the chances of finding positive mosquitoes. However, Ae. aegypti collections are usually small, and in many cases, it would be easier to Advances in arbovirus detection, characterization pool the mosquitoes (or alternatively, squash them into and data interpretation FTA® cards [68]) and process them by molecular Next-generation sequencing for the detection of methods. arboviruses Like any system, sugar-based surveillance has some Traditionally, diagnostic assays utilised in arbovirus limitations. Perhaps its main limitation is that the cycle surveillance programs only screen for characterised threshold (C ) values obtained by real time RT-PCR are endemic and enzootic viruses. Because virus specific high (> 30 cycles), reflecting the relatively small amount primers and probes are used for molecular diagnos- of saliva expectorated by mosquitoes [69]. Additionally, tics, it is likely that many other viruses, whether this method will only detect positive mosquitoes after pathogenic or not, remain undetected. Metagenomic the extrinsic incubation period which, depending on the analysis using next-generation sequencing (NGS), al- virus, can last from two to 14 days. Thus, the proportion lows for the simultaneous identification of viruses, of mosquitoes in a population that survive to transmit mosquito species, and endosymbionts, such as Wolba- the virus can be quite low. In order to increase mosqui- chia, from a single mosquito in a single reaction [78] toes feeding on the FTA® cards, trapped mosquitoes without prior sequence knowledge. This approach re- must be kept alive in the trap for as long as possible. lies on bioinformatics tools to analyse the millions of The SMACK was developed to include a water reservoir sequence reads [79–81] and the availability of in the trap to increase humidity, the lack of which can high-quality sequence databases to analyse the large be a problem in remote and arid locations. To save on and complex datasets generated. In Australia, viral reagent costs, some agencies will wait until they have metagenomics has been used for the identification of sufficient samples to batch together, which can extend multiple arboviruses, including novel rhabdoviruses, the turnaround time. Finally, sugar-based surveillance bunyaviruses [82]and mesoniviruses [83] from field does not provide data on the mosquito species that ex- collected mosquitoes. pectorated the virus. Instead, detection of virus on a At this stage, NGS methods have some disadvantages FTA® removed from a trap could be used to trigger in- compared with other molecular methods of virus detec- tensive trapping to collect mosquitoes for pooling and tion. NGS is less sensitive than qRT-PCR for the detec- processing to provide information on potential vectors tion of samples with low virus titres [84]. At present, the at a given time point or location. costs associated with NGS are higher than the cost of A potential way to increase sensitivity of sugar-based qRT-PCR, and its associated equipment has a relatively surveillance systems is through the collection and analysis large laboratory footprint. It also requires intimate bio- of mosquito excreta. When mosquitoes feed on a sucrose informatics knowledge and reference sequence databases solution it takes approximately 30 min for it to reach the to analyse the data produced. Over the past years, there midgut, after which excreta is ejected from the anus [70]. has been advancement in the hardware used for NGS, In terms of pathogen detection, the focus has mainly been with equipment getting smaller and cheaper. The first on the detection of filarial nematodes, such as Brugia hand-held portable sequencer (MinION) is already avail- malayi [71]and Plasmodium vivax [72]. In the late 1920s, able on the market. This platform reduces processing de Beaurepaire Aragão and da Costa Lima performed a time significantly (e.g. < 6 hours for detection of CHIKV series of experiments in which they infected rhesus from blood samples [85]). Even with operational chal- macaques with the excreta collected from YFV infected lenges, the MinION’s high portability and low energy re- Ae. aegypti [73–75]. Laboratory-based experiments have quirements have enabled its use in extreme field recently demonstrated that Ae. aegypti with a dissemi- conditions [86] and it has been used to investigate out- nated infection excrete DENV RNA, which can be de- breaks of Ebola [87] and Salmonella [88]. It has recently tected through qRT-PCR [76]. The rate of detection was been demonstrated that the MinION can be used for higher in excreta samples, 89%, compared with 33% for metagenomic arbovirus detection from infected mosqui- saliva samples. This suggests that collection of excreta toes [89], so it could be used during arbovirus outbreaks. from trapped mosquitoes could enhance the sensitivity of Although the MinION still has limitations, such as high current sugar-based surveillance systems. This is not sur- error rates and requirement for an internet connection prising, given that mosquitoes excrete considerably more for base calling, technologies like this, together with fluid than they salivate (~1.5 μl[77] vs 4.7 nl [69]). Inte- lower reagent costs, will be crucial in making sequencing gration of excreta collection into current surveillance accessible in the field in the near future. Ramírez et al. Parasites & Vectors (2018) 11:320 Page 7 of 12 Xenosurveillance This system has been successful at reducing dengue in Mosquitoes have the potential to act as environmental the municipalities that have adopted it. samplers (“biological syringes”) that feed on the blood of In the age of mobile phones, social media and internet, a variety of vertebrate hosts. Xenosurveillance offers an citizen science will undoubtedly play an important role alternative to directly sampling hosts, a process that is in disease surveillance in general. In Spain, Mosquito time consuming and requires individual informed con- Alert was implemented as a system to collect reports of sent in the case of humans or animal ethics approval, in invasive Ae. albopictus. To date, it has more than 30,000 the case of veterinary pathogens. Mosquitoes can be registered participants [102]. As a part of the GLOBE used as a proxy for syringe sampling of small animals for project sponsored by NASA, Mosquito Habitat Mapper virus titer determination [90]. This approach has mainly merges data generated by citizens with satellite-based re- been used to study vector-borne pathogens, such as filar- search [103]. Interestingly, with minimal training, the ial parasites [91] or apicomplexans [92]. For example, in data generated by programmes like these is considered Sri Lanka, xenosurveillance has been successfully used as reliable as data collected by experts [104]. Mobile to map areas with persistent Wuchereria bancrofti phones, even low-end ones, can also be used as acoustic after mass drug administration programmes [93]. Fur- sensors to identify mosquito species [105]. All these ini- thermore, it has been possible to detect DENV from tiatives will allow large-scale data acquisition, which is (non-competent) Anopheles stephensi mosquitoes 24 h critical for adequate mosquito control. after ingestion [94]. In addition to viruses that ac- Over the past 20 years, single device detection plat- tively replicate in them, engorged mosquitoes poten- forms for clinical and environmental analyses have been tially possess viruses or other pathogens that do not rapidly evolving. A promising technique for integration replicate in them but might be present in hosts they feed into surveillance programmes is the use of microfluidic upon [95]. Xenosurveillance monitors these potential devices [106] and biosensors [107] which are designed to non-vector borne human and animal pathogens [96]by process very small volumes of liquid, requiring minimal performing nucleic acid detection or vector enabled meta- amount of sample and reagents to yield results in mi- genomics [97] on mosquito samples. Mosquitoes have nutes [108, 109]. Some applications of these devices in- been successfully used to monitor non-mosquito borne clude diagnosis of infections caused by DENV [110–112] pathogens such H5N1 influenza virus [98], Epstein-Barr and CHIKV [113] from clinical samples, detection of virus, canine distemper virus [96], human herpesvirus, hu- DENV NS1 antigen from pools of mosquitoes [114] and man papillomaviruses, anelloviruses and circoviruses, genotyping of closely related Anopheles species [115]. among others [95]. One of the main limitations of xenosurveillance is the Conclusions difficulty in collecting sufficient blood engorged mosqui- Over the past decade, there have been key scientific ad- toes for analysis. Some of the methods to collect engorged vances in arbovirus surveillance, particularly with regard mosquitoes (i.e. use of an aspirator) are labour intensive to sample collection, virus detection and data analysis. and can be intrusive, especially when sampling inside Table 3 summarises the relative advantages and disadvan- houses and villages [99]. To circumvent this issue, mos- tages of current and emerging surveillance methodologies. quito excreta could be used to provide the template for Alternative samples for virus detection, such as mosquito xenosurveillance. Indeed, hepatitis B virus, which does not excreta, may enable more sensitive detection of arbovi- replicate in the vector, has been detected in mosquito ex- ruses than existing methodologies. It has been proposed creta by RT-PCR and Southern Blot up to 7 days after the that we are on the cusp of a revolution in genomic epi- ingestion of an infectious blood meal [100]. demiology [116]. With NGS technologies becoming more accessible in the near future, they will enable the collec- tion of real-time in-depth genetic information on circulat- Emerging technology ing arboviruses before or during an outbreak. There is still Integration of data acquisition, storage and sharing room for improvement of surveillance systems used in re- methodologies, such as cloud networks and geographic mote locations where surveillance coverage is limited by information systems, will form an integral component of cost and limited access to sites. Use of other sources of surveillance and control programmes. An example of CO in mosquito traps (such as fermentation using yeast) this is the Intelligent Dengue Monitoring technology [117]or CO -free systems could provide an alternative in (MI-Dengue) developed in Brazil [101]. MI-Dengue con- areas where dry ice or pressurized gas cylinders are not sists of an array of tools to collect gravid Ae. aegypti fe- available. Deployment of in-field portable molecular la- males, collect field data, detect virus and create boratories or point of care assays could provide same-day georeferenced infestation maps that are available in real assessment of arbovirus circulation and rapid response in time, providing information to optimize vector control. these locations [118]. In the future, other technologies, Ramírez et al. Parasites & Vectors (2018) 11:320 Page 8 of 12 Table 3 Summary of traditional and novel arbovirus surveillance methods Method Advantages Disadvantages Application Monitoring human and animal Uses data that is already being Overlap of clinical symptoms National disease surveillance disease collected by hospitals, health within arboviruses and other databases practitioners, and animal pathogens. Not ideal for early health personnel warning since active transmission will be already occurring Sentinel animals Can act as an early warning Animals can be amplifying Routine surveillance, inform system hosts. High costs associated control strategies with animal rearing. Cross reactivity between closely related arboviruses when using serological assays Virus isolation from pools of Increases virus titer allowing Time consuming. Requires Routine surveillance, virus mosquitoes for genotypic and phenotypic special infrastructure identification, inform control characterization (biological containment). strategies Requires a cold chain Virus detection in pools of Allows high throughput Will only detect RNA from Routine surveillance, research, mosquitoes using molecular screening. High sensitivity viruses that the assays were inform control strategies assays designed to detect. Requires special infrastructure Virus detection in pools of Rapid. Does not require Lower sensitivity than Routine surveillance in low mosquitoes using rapid specialized equipment. Lower molecular methods resource settings antigen detection assays cost Sugar-based surveillance Does not require a cold chain. Relies on a nanoliter amounts Routine surveillance, ideal for Only 1-2 samples per trap are of expectorate. Mosquitoes remote locations tested potentially compared need to be kept alive for as with 1000s of mosquitoes long as possible to increase using other methods of sur- feeding on cards. Cannot be veillance. Better estimation of used to incriminate mosquito transmission risk species as vectors. Requires special infrastructure Next-generation sequencing of Does not require prior High cost. Requires Research, virus discovery mosquito samples information (will detect any bioinformatics knowledge. arbovirus present in the Requires special infrastructure sample) Xenosurveillance Mosquito acts as an Blood engorged mosquitoes Research and surveillance of environmental sampler. Allows are difficult to collect arboviruses and other detection of viruses that do pathogens not replicate in the mosquito such as unmanned aerial vehicles (UAVs) could be used to Abbreviations DENV: Dengue virus; JEV: Japanese encephalitis virus; WNV: West Nile virus; automate sample collection in difficult to access locations CHIKV: Chikungunya virus; ZIKV: Zika virus; YFV: Yellow fever virus; SLEV: St. increasing the coverage of surveillance. Regardless of the Louis encephalitis virus; RRV: Ross River virus; BFV: Barmah Forest virus; surveillance system, there are always going to be issues MVEV: Murray Valley encephalitis virus; BTV: Blue tongue virus; RVFV: Rift Valley fever virus; EEEV: Eastern equine encephalitis virus; WEEV: Western and limitations, which can vary between jurisdictions. equine encephalitis virus; ISF: insect-specific flaviviruses; IgG: immunoglobulin Currently, the extent of arbovirus surveillance varies be- G; PCR: polymerase chain reaction; RT-PCR: reverse-transcription polymerase tween countries and even states with many jurisdictions chain reaction; RNA: ribonucleic acid; FTA®: Flinders Associate Technologies; PBT: passive box trap; SMACK: sentinel mosquito arbovirus capture kit; lacking any form of monitoring. There is a need for shar- C : cycle threshold; GAT: gravid Aedes trap; NGS: next-generation sequencing; ing of arbovirus surveillance intelligence between public UAV: unmanned aerial vehicle health agencies at regional level as a means to apply better control measures. Moreover, the implementation issues Acknowledgments that might arise from new approaches cannot be underes- The authors would like to acknowledge Brian J. Johnson and Kyran M. Staunton for their feedback on previous drafts of this article. timated. Agencies that are familiar with set methodologies may be reluctant to adopt new technologies or not have the capacity to implement change. Because of this, when Funding ALR was supported by a doctoral scholarship granted by the Australian designing new arbovirus surveillance methodologies, there Institute of Tropical Health and Medicine, James Cook University QLD, should be a clear understanding of the needs and limita- Australia. 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The resting box technique for the sampling of Culiseta melanura (Coquillet). Proc N J Mosq Exterm Assoc. 1971:122–5. 159. Komar N, Pollack RJ, Spielman A. A nestable fiber pot for sampling resting mosquitoes. J Am Mosq Control Assoc. 1995;11:463–467. 160. Panella NA, Crockett RJ, Biggerstaff BJ, Komar N. The centers for disease control and prevention resting trap: a novel device for collecting resting mosquitoes. J Am Mosq Control Assoc. 2011;27:323–5. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Parasites & Vectors Springer Journals

Searching for the proverbial needle in a haystack: advances in mosquito-borne arbovirus surveillance

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Biomedicine; Parasitology; Entomology; Tropical Medicine; Infectious Diseases; Veterinary Medicine/Veterinary Science; Virology
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Abstract

Surveillance is critical for the prevention and control of mosquito-borne arboviruses. Detection of elevated or emergent virus activity serves as a warning system to implement appropriate actions to reduce outbreaks. Traditionally, surveillance of arboviruses has relied on the detection of specific antibodies in sentinel animals and/or detection of viruses in pools of mosquitoes collected using a variety of sampling methods. These methods, although immensely useful, have limitations, including the need for a cold chain for sample transport, cross- reactivity between related viruses in serological assays, the requirement for specialized equipment or infrastructure, and overall expense. Advances have recently been made on developing new strategies for arbovirus surveillance. These strategies include sugar-based surveillance, whereby mosquitoes are collected in purpose-built traps and allowed to expectorate on nucleic acid preservation cards which are submitted for virus detection. New diagnostic approaches, such as next-generation sequencing, have the potential to expand the genetic information obtained from samples and aid in virus discovery. Here, we review the advancement of arbovirus surveillance systems over the past decade. Some of the novel approaches presented here have already been validated and are currently being integrated into surveillance programs. Other strategies are still at the experimental stage, and their feasibility in the field is yet to be evaluated. Keywords: Arboviruses, Surveillance, Mosquito, Sentinel animals, Honey-based surveillance, Next-generation sequencing Background Africa [4] and Brazil [5] have highlighted the continuing Arthropod-borne viruses (arboviruses) transmitted by threat emerging and re-emerging arboviruses pose. mosquitoes are of public health and veterinary import- With the exception of YFV [6] and JEV [7], there are ance globally causing disease syndromes including en- currently few vaccines or antiviral drugs available against cephalitis, viral haemorrhagic disease and arthritis. most of these viruses. Thus, prevention and control of Dengue viruses (DENVs) alone cause an estimated 96 most arboviruses is almost solely reliant on effective million clinical cases a year, especially in the tropics and mosquito management. This can be enhanced by sur- sub-tropics [1]. The flaviviruses, Japanese encephalitis veillance, where detection of elevated or emergent virus virus (JEV) and West Nile virus (WNV), are major activity serves as a warning system to implement appro- causes of viral encephalitis throughout their geograph- priate actions to reduce the severity and duration of out- ical range. Recently, the expansion of chikungunya breaks. However, designing an appropriate arbovirus (CHIKV) [2] and Zika (ZIKV) [3] viruses in the Western surveillance system is challenging. Arboviruses have Hemisphere, and the yellow fever (YFV) outbreaks in complex transmission cycles with dual-host tropism: they replicate in vertebrate hosts (such as birds or mammals) and arthropod hematophagous vectors (such as mosqui- toes or ticks) [8]. This complexity needs to be accounted * Correspondence: ana.ramirez1@my.jcu.edu.au for, and an ideal surveillance system should rely on differ- College of Public Health, Medical and Veterinary Sciences, James Cook University, PO Box 6811, Cairns, QLD 4870, Australia ent sources of information (Fig. 1), and can include Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. Ramírez et al. Parasites & Vectors (2018) 11:320 Page 2 of 12 Fig. 1 Transmission cycles of arboviruses and different strategies for arbovirus surveillance meteorological data, evidence of virus infection in verte- for WNV [14]. In Argentina [15] and Brazil [16], dead brate hosts, entomological surveys, virus detection in vec- howler monkeys acted as an early warning for sylvatic tors, and reports of human or animal disease. The scale of transmission of YFV and prompted vaccination cam- surveillance can vary regionally [9] and is particularly paigns in the human population in 2008 and 2017, challenging in remote locations, or in areas with limited respectively. resources and infrastructure. A major limitation of monitoring human and animal Given the broadness of this subject, few attempts have cases is that confirmatory laboratory testing is not avail- been made to provide a synthesis of arbovirus surveil- able in many limited resource countries, so arboviral dis- lance methods. The objective of this review is to de- ease is diagnosed on clinical symptoms. However, scribe the development and implementation of symptoms can overlap between arboviruses, as well as mosquito-borne arbovirus surveillance strategies. First, with non-arbovirus pathogens, complicating their clin- we evaluate traditional methods that have been com- ical diagnosis. Furthermore, most arbovirus infections monly used where arboviruses are a public health threat, are mild, or sub-clinical, which may lead to them being then outline and assess recently developed methodolo- under-reported. Ultimately, using human and animal gies, before identifying future research needs. case data is not ideal, since it indicates that active trans- mission is already occurring. Methods for arbovirus surveillance Monitoring human and animal disease Vertebrate host arbovirus surveillance: sentinel animals Human or animal case surveillance relies on hospitals, Sentinel animals provide evidence of virus activity and laboratories and health practitioners notifying public increased risk to the target animal or human population health authorities of confirmed or suspected cases of [17]. For this, immunologically naïve animals are de- arbovirus infection that occur in the population. Almost ployed in a specific location, bled on a defined schedule, every state in the United States conducts surveillance of and tested for the presence of virus-specific antibodies human WNV cases as a part of the national arbovirus as an indication of exposure. Virus isolation or molecu- surveillance system, ArboNET [10], whilst in Australia, lar detection on pre-seroconversion blood samples can human arbovirus disease notifications are monitored provide an isolate and/or a sequence for genotypic ana- using the National Notifiable Disease Surveillance Sys- lysis of circulating virus strains [18]. A suitable sentinel tem (NNDSS) [11]. These surveillance systems require animal should: (i) be susceptible to the monitored virus; strict case definitions and laboratory diagnostic testing (ii) develop an antibody response that can be detected in criteria, as well as demographic, clinical, laboratory and serological assays; (iii) have low morbidity and mortality; epidemiological information [12]. In the summer and (iv) be attractive to the vector; (v) be easy to handle; and autumn of 1999, reports of dead crows played a critical (vi) allow for multiple sampling [12]. role in identifying the outbreak of WNV in New York Different vertebrate species are used as sentinels [13]. With bird cases often preceding human cases by up (Table 1) and choice of animal is dependent on the tar- to 3 months, it served as an ideal early warning system get virus. In terms of WNV surveillance, some studies Ramírez et al. Parasites & Vectors (2018) 11:320 Page 3 of 12 Table 1 Animal species that have been used as sentinels for arbovirus surveillance Animal Virus Example location References Chickens WNV USA, UK [119, 120] SLEV USA [121] MVEV, WNV Australia [122] KUN Pheasants WNV, SLEV, EEEV USA [123, 124] Pigs JEV Japan, Australia, Thailand [125–127] Dogs WNV USA, Africa [128, 129] JEV Japan, Thailand [130, 131] Sheep and goats RVFV Africa, Saudi Arabia [132–134] Cattle BTV, Akabane Australia, Papua New Guinea, Japan [135–137] Horses EEEV, WEEV Argentina [138] WNV, SLE Colombia [139] Hamsters EEEV, VEEV USA, Central and South America [140–143] Non-human primates YFV Brazil, Argentina [144–147] Abbreviations: WNV, West Nile virus; SLEV, St. Louis encephalitis virus; MVEV, Murray Valley encephalitis virus; WNV , West Nile virus (Kunjin subtype); EEEV, KUN eastern equine encephalitis virus; JEV, Japanese encephalitis virus; RVFV, Rift Valley fever virus; BTV, bluetongue virus; WEEV, western equine encephalitis virus; VEEV, Venezuelan equine encephalitis virus; YFV, yellow fever virus have suggested that the use of sentinel chickens is the are mobile, it is difficult to determine exactly when and most sensitive indicator of virus activity, when compared where an animal acquired the infection, especially since with other methods, such as detection of seroconversion IgG antibodies are present for the life of the animal. in wild birds and virus isolation from mosquito pools [19]. Whilst they can undoubtedly serve as an early Mosquito-based arbovirus surveillance warning system, in some areas of the USA, sentinel Mosquito-based arbovirus surveillance monitors vector chickens to monitor WNV have proven unsuccessful, populations and virus infection prevalence within them. since seroconversions were detected only after the onset Mosquitoes are collected, identified, pooled by species of human cases [20, 21]. or other taxonomic grouping, and sent to the laboratory Even though sentinel animal surveillance enables the where they are tested for virus infection status. There timely detection of circulating arboviruses, it also comes are different strategies for mosquito collection. In areas with limitations. In many cases, the locations of enzootic with low-level mosquito infections or early in the trans- arbovirus foci are unknown or difficult to access. Thus, mission season, efforts should be directed towards per- animals are placed near towns, which may be too far forming targeted surveillance at “hotspots” where a high from virus foci to detect elevated activity [22]. Further- likelihood of arbovirus presence is suspected; as vector more, some animals serve as amplifying hosts (i.e. pigs populations increase later in the season, the number of for JEV) increasing the risk of transmission to humans sampling sites should be expanded for broader monitor- [23]. Additionally, the cost of rearing and replacing sen- ing [29]. There are a variety of commercial traps de- tinel animals, especially in remote locations, can be pro- signed to collect mosquitoes, the design of which and hibitive [24, 25], and bleeding large animals presents a application have been comprehensively reviewed else- workplace health and safety hazard [26]. There are also where [30, 31]. It is essential that the selection of the ethical considerations associated with the use of sentinel collection method takes into consideration the physio- animals [27]. Finally, closely related viruses (i.e. JEV, logical and behavioural characteristics of the studied WNV and Murray Valley encephalitis virus (MVEV)) vector [32] (Table 2). can cross-react in some serological assays, requiring A variety of methods have been utilized for detection confirmation by other methods to obtain unequivocal of arboviruses in captured mosquitoes. Historically, results [28]. arbovirus isolations were conducted in animals, such as Another approach to vertebrate host surveillance relies suckling mice and chickens. With the development and on monitoring wild vertebrates or livestock, which are establishment of cell lines, virus isolation in cell culture captured, sampled and released [12]. However, one of became the gold standard for arbovirus detection from the biggest issues with surveillance of these animals is pools of mosquitoes. This method can only detect viable the cross-reaction between antibodies and the interpret- viruses, so a cold chain keeping samples at ultralow tem- ation of the results. Given that many of these animals peratures during transport needs to be maintained to Ramírez et al. Parasites & Vectors (2018) 11:320 Page 4 of 12 Table 2 Collection methods commonly used for mosquito-based arbovirus surveillance Mosquito Collection method Advantages Disadvantages References behaviour Host seeking Human-landing catches Larger collections than resting or oviposition Most traps require batteries or AC power to [148] collections. Collections can be increased by operate. Depending on environmental BG Sentinel [149] using CO or chemical lures conditions, the fan components are prone to malfunction. Require CO as the primary CDC-light trap 2 [150] attractant EVS-trap [151] Mosquito Magnet™ [152] Animal baited traps [153–155] Resting CDC-backpack aspirator More blood fed mosquitoes collected, ideal Labour intensive and inefficient mosquito [156] for blood meal analysis capture Prokopack [157] Resting boxes [158–160] Oviposition Sticky ovitraps Mosquitoes have bloodfed and thus a higher Smaller collections than other methods, thus [161–163] probability of detecting positive mosquitoes. all mosquitoes can be easily processed Gravid Aedes trap (GAT) [66] Targets Aedes-borne viruses such as DENV and CHIKV CDC-gravid trap [164] Although this method has been used for arbovirus studies in the past, it has considerable drawbacks, including the risk of infection to the collector, which is considered unethical even illegal in some countries Abbreviations: CDC, Centers for Disease Control and Prevention; EVS, Encephalitis virus surveillance preserve virus infectivity [33]. Maintenance of a cold arbovirus of human (and veterinary) importance, with chain requires the use of dry ice or liquid nitrogen ship- some even available in multiplex format [41]. In spite of pers in the field, which can be logistically challenging. this, it is important to note that RT-PCR and qRT-PCR Virus isolation is time consuming and obtaining defini- will only pick up RNA from viruses that the primers and tive results can take weeks, which defeats the purpose of probes were designed to detect [42]. Historically, one of using it for early warning. Some viruses do not replicate the main drawbacks of this method has been its high in- on common cell lines used in the laboratory. This can stallation and reagent costs, limiting its use in be the case for previously unrecognized or unknown vi- low-resource settings. However, recently, costs associ- ruses, such as insect-specific flaviviruses (ISF) that do ated with qRT-PCR have dropped considerably making not grow in vertebrate cells [34]. Virus isolation can be it an accessible alternative for routine screening. expensive and requires special infrastructure and trained Rapid antigen detection assays were initially developed personnel. However, even with these limitations, virus to test clinical samples but have proven to be a useful isolation is still an important method for arbovirus diag- tool to test mosquito pools in the field [43]. These assays nostics, as it increases viral titer, which allows for full allow for qualitative detection of arboviruses, and have genome sequencing and provides viruses for phenotypic the advantage of being rapid, without the need for spe- characterization. cialized equipment. Currently, there are tests commer- Nucleic acid detection using RT-PCR has become one cially available for a variety of viruses including CHIKV of the most popular methods of virus detection and has [44], DENV [45] and WNV [43], among others. In potentially displaced virus isolation as the new gold Singapore [46] and Malaysia [47], a dengue NS1 rapid standard. Real time quantitative RT-PCR (qRT-PCR) test has been used to detect infected mosquitoes as part platforms, such as TaqMan®, are ideal for routine testing of a routine surveillance programme. These tests have of mosquitoes, since they reduce processing time signifi- shown high specificity for the target virus, although cantly (sometimes to less than an hour), allowing for some assays have reduced sensitivity when compared high throughput screening [35, 36]. Since these assays with molecular methods [48, 49]. However, although detect both infectious virus and RNA, they have com- they may provide an underestimate of infection rate, parable or better sensitivity than virus isolation [37]. De- they provide a first screen and have applicability in re- pending on the protocol or application, these techniques gions without access to more resource intensive or ex- enable the detection of one infected individual from a pensive diagnostic capacity. pool of up to 5000 non-infected mosquitoes [38, 39]. Traditional mosquito-based surveillance systems that Additionally, although a cold chain is still recommended, target processing of pools of mosquitoes come with in- it has been possible to detect viral RNA from dead mos- herent limitations. Mosquito populations often have very quitoes kept for several weeks in hot and humid condi- low carriage rates, whereby only one in 1000 mosquitoes tions by qRT-PCR [33, 39, 40]. Currently, a variety of is actually infected [50]. To increase the probability of qRT-PCR assays exist for the detection of almost every detection, large numbers of mosquitoes are required, Ramírez et al. Parasites & Vectors (2018) 11:320 Page 5 of 12 resulting in numerous mosquitoes to identify, pool and Free-standing sugar bait stations have the potential to test, increasing laboratory costs and turnaround time. be used instead of CO -baited traps [59]. These stations Additionally, many traps require attractants, such as consist of a dental wick soaked in sucrose solution and a CO , to increase collections. This comes in the form of floral lure, such as phenyl acetaldehyde. Mosquitoes dry ice or pressurized cylinders, which may not be read- lured to the station feed on the wick, which is tested for ily available, or only allow overnight deployment of the expectorated viral RNA. The sugar bait stations do not trap. A cold chain of storage at < -50 °C is required to require CO or electricity, so a number of stations can preserve the integrity of the virus for detection, which be deployed simultaneously, thus increasing geographical can be a challenge in remote locations. Finally, special- coverage. In a proof of concept, the sugar bait stations ized laboratory equipment and infrastructure is required detected WNV before sentinel animals seroconverted in for diagnostics, which might not be available in develop- California. However, this method appears more effica- ing countries. cious in arid habitats, probably because of lack of com- petition with other sucrose sources, such as floral nectars. As sugar bait stations facilitate increased geo- Novel methods for arbovirus surveillance graphical coverage, they may have higher costs associ- The majority of mosquito species feed on carbohydrates ated with analysing an increased number of samples, (i.e. flower nectar, honeydew or rotting fruit) which are although this would be offset by savings by not having to the primary energy source of their diet [51]. One excep- use CO baited light traps. tion is Ae. aegypti, which appears to obtain enough en- Sugar-based surveillance has several advantages over ergy from blood and rarely feeds on sugar in domestic traditional methods. When mosquito populations are el- environments [52]. The ingestion of carbohydrates is im- evated, sorting becomes time consuming, and a high portant for the survival of the mosquito, and plays an in- number of pools can overwhelm laboratory capacity. direct role in disease transmission, allowing an infected When combined, these issues can reduce the ability to female to live long enough to become infective [53]. It provide results in a timely manner. Sugar-based methods was hypothesized by Doggett et al. [54] and confirmed potentially overcome these issues, since only 1-2 FTA® by van den Hurk et al. [55], that infected mosquitoes ex- cards per trap are tested, compared to a variable number pectorate virus while sugar feeding, which can be de- of mosquito pools. As only transmitting mosquitoes will tected using molecular assays. This finding led to the yield positive results, the presence of virus in saliva ex- development of novel sugar-based approaches for the pectorate is a better estimate of transmission risk. FTA® detection of arboviruses in mosquitoes in the field. This cards can preserve viral RNA for up to 28 days [56], system integrates purpose-built CO -baited box traps, making this an ideal alternative for surveillance in re- which house nucleic acid preservation cards (Flinders mote or difficult to access locations, where regular ser- Technology Associates, FTA® cards) soaked in honey vicing of traps is not feasible. Results suggest that and on which mosquitoes feed and expectorate onto sugar-based surveillance is a more sensitive indicator of [56]. The FTA® cards inactivate any expectorated viruses arbovirus activity than sentinel animals. In northern and preserve the liberated RNA. The cards are then sent Australia, it has been possible to detect WNV before KUN to the laboratory in the post without requirement of a sentinel animal seroconversions [60]. However, a com- cold-chain, where they are screened for viruses using parison of the sugar-based surveillance system with molecular assays. existing strategies still needs to be thoroughly evaluated. Commonly used traps employed to collect mosquitoes Sugar-based surveillance, using either SMACK or EVS (i.e. CDC-light trap and Encephalitis Virus Surveillance, traps, has been successfully incorporated into existing EVS, trap) require batteries to operate which can be lo- surveillance programs in Australia, with multiple detec- gistically challenging. To circumvent this limitation, a tions of MVEV, WNV , RRV, BFV, Edge Hill virus KUNV non-powered CO -baited passive box trap (PBT) was de- and Stratford virus [61–64]. veloped by Ritchie et al. [57] to collect and house mos- Honey-soaked FTA® cards have the potential to be in- quitoes. A variation of the PBT, the sentinel mosquito tegrated into surveillance of Ae. aegypti-borne arbovi- arbovirus capture kit (SMACK) was developed to in- ruses. The cards have been used in Biogents sentinel crease mosquito survivorship and consequently increase traps (BGS traps) and modified double sticky ovitraps the probability of infected mosquitoes feeding on the for the detection of CHIKV in French Guiana [65]. The FTA® card [58]. Although designed for weekly or fort- approach appeared time consuming with only one nightly servicing, the SMACK has demonstrated similar CHIKV positive FTA® card out of 234 analysed. Traps trap efficacy to the CDC-light trap and EVS trap in over- that are more efficient at collecting Ae. aegypti may be night collections, making it an alternative to traps that able to increase trap collections, thus increasing the like- require batteries to operate. lihood of detecting virus. For instance, the Gravid Aedes Ramírez et al. Parasites & Vectors (2018) 11:320 Page 6 of 12 Trap (GAT) [66] collects 2.4 times more Ae. aegypti and systems would require modification of current trap de- significantly more gravid females than double sticky ovi- signs to selectively capture mosquito excreta. traps [67], which could increase the chances of finding positive mosquitoes. However, Ae. aegypti collections are usually small, and in many cases, it would be easier to Advances in arbovirus detection, characterization pool the mosquitoes (or alternatively, squash them into and data interpretation FTA® cards [68]) and process them by molecular Next-generation sequencing for the detection of methods. arboviruses Like any system, sugar-based surveillance has some Traditionally, diagnostic assays utilised in arbovirus limitations. Perhaps its main limitation is that the cycle surveillance programs only screen for characterised threshold (C ) values obtained by real time RT-PCR are endemic and enzootic viruses. Because virus specific high (> 30 cycles), reflecting the relatively small amount primers and probes are used for molecular diagnos- of saliva expectorated by mosquitoes [69]. Additionally, tics, it is likely that many other viruses, whether this method will only detect positive mosquitoes after pathogenic or not, remain undetected. Metagenomic the extrinsic incubation period which, depending on the analysis using next-generation sequencing (NGS), al- virus, can last from two to 14 days. Thus, the proportion lows for the simultaneous identification of viruses, of mosquitoes in a population that survive to transmit mosquito species, and endosymbionts, such as Wolba- the virus can be quite low. In order to increase mosqui- chia, from a single mosquito in a single reaction [78] toes feeding on the FTA® cards, trapped mosquitoes without prior sequence knowledge. This approach re- must be kept alive in the trap for as long as possible. lies on bioinformatics tools to analyse the millions of The SMACK was developed to include a water reservoir sequence reads [79–81] and the availability of in the trap to increase humidity, the lack of which can high-quality sequence databases to analyse the large be a problem in remote and arid locations. To save on and complex datasets generated. In Australia, viral reagent costs, some agencies will wait until they have metagenomics has been used for the identification of sufficient samples to batch together, which can extend multiple arboviruses, including novel rhabdoviruses, the turnaround time. Finally, sugar-based surveillance bunyaviruses [82]and mesoniviruses [83] from field does not provide data on the mosquito species that ex- collected mosquitoes. pectorated the virus. Instead, detection of virus on a At this stage, NGS methods have some disadvantages FTA® removed from a trap could be used to trigger in- compared with other molecular methods of virus detec- tensive trapping to collect mosquitoes for pooling and tion. NGS is less sensitive than qRT-PCR for the detec- processing to provide information on potential vectors tion of samples with low virus titres [84]. At present, the at a given time point or location. costs associated with NGS are higher than the cost of A potential way to increase sensitivity of sugar-based qRT-PCR, and its associated equipment has a relatively surveillance systems is through the collection and analysis large laboratory footprint. It also requires intimate bio- of mosquito excreta. When mosquitoes feed on a sucrose informatics knowledge and reference sequence databases solution it takes approximately 30 min for it to reach the to analyse the data produced. Over the past years, there midgut, after which excreta is ejected from the anus [70]. has been advancement in the hardware used for NGS, In terms of pathogen detection, the focus has mainly been with equipment getting smaller and cheaper. The first on the detection of filarial nematodes, such as Brugia hand-held portable sequencer (MinION) is already avail- malayi [71]and Plasmodium vivax [72]. In the late 1920s, able on the market. This platform reduces processing de Beaurepaire Aragão and da Costa Lima performed a time significantly (e.g. < 6 hours for detection of CHIKV series of experiments in which they infected rhesus from blood samples [85]). Even with operational chal- macaques with the excreta collected from YFV infected lenges, the MinION’s high portability and low energy re- Ae. aegypti [73–75]. Laboratory-based experiments have quirements have enabled its use in extreme field recently demonstrated that Ae. aegypti with a dissemi- conditions [86] and it has been used to investigate out- nated infection excrete DENV RNA, which can be de- breaks of Ebola [87] and Salmonella [88]. It has recently tected through qRT-PCR [76]. The rate of detection was been demonstrated that the MinION can be used for higher in excreta samples, 89%, compared with 33% for metagenomic arbovirus detection from infected mosqui- saliva samples. This suggests that collection of excreta toes [89], so it could be used during arbovirus outbreaks. from trapped mosquitoes could enhance the sensitivity of Although the MinION still has limitations, such as high current sugar-based surveillance systems. This is not sur- error rates and requirement for an internet connection prising, given that mosquitoes excrete considerably more for base calling, technologies like this, together with fluid than they salivate (~1.5 μl[77] vs 4.7 nl [69]). Inte- lower reagent costs, will be crucial in making sequencing gration of excreta collection into current surveillance accessible in the field in the near future. Ramírez et al. Parasites & Vectors (2018) 11:320 Page 7 of 12 Xenosurveillance This system has been successful at reducing dengue in Mosquitoes have the potential to act as environmental the municipalities that have adopted it. samplers (“biological syringes”) that feed on the blood of In the age of mobile phones, social media and internet, a variety of vertebrate hosts. Xenosurveillance offers an citizen science will undoubtedly play an important role alternative to directly sampling hosts, a process that is in disease surveillance in general. In Spain, Mosquito time consuming and requires individual informed con- Alert was implemented as a system to collect reports of sent in the case of humans or animal ethics approval, in invasive Ae. albopictus. To date, it has more than 30,000 the case of veterinary pathogens. Mosquitoes can be registered participants [102]. As a part of the GLOBE used as a proxy for syringe sampling of small animals for project sponsored by NASA, Mosquito Habitat Mapper virus titer determination [90]. This approach has mainly merges data generated by citizens with satellite-based re- been used to study vector-borne pathogens, such as filar- search [103]. Interestingly, with minimal training, the ial parasites [91] or apicomplexans [92]. For example, in data generated by programmes like these is considered Sri Lanka, xenosurveillance has been successfully used as reliable as data collected by experts [104]. Mobile to map areas with persistent Wuchereria bancrofti phones, even low-end ones, can also be used as acoustic after mass drug administration programmes [93]. Fur- sensors to identify mosquito species [105]. All these ini- thermore, it has been possible to detect DENV from tiatives will allow large-scale data acquisition, which is (non-competent) Anopheles stephensi mosquitoes 24 h critical for adequate mosquito control. after ingestion [94]. In addition to viruses that ac- Over the past 20 years, single device detection plat- tively replicate in them, engorged mosquitoes poten- forms for clinical and environmental analyses have been tially possess viruses or other pathogens that do not rapidly evolving. A promising technique for integration replicate in them but might be present in hosts they feed into surveillance programmes is the use of microfluidic upon [95]. Xenosurveillance monitors these potential devices [106] and biosensors [107] which are designed to non-vector borne human and animal pathogens [96]by process very small volumes of liquid, requiring minimal performing nucleic acid detection or vector enabled meta- amount of sample and reagents to yield results in mi- genomics [97] on mosquito samples. Mosquitoes have nutes [108, 109]. Some applications of these devices in- been successfully used to monitor non-mosquito borne clude diagnosis of infections caused by DENV [110–112] pathogens such H5N1 influenza virus [98], Epstein-Barr and CHIKV [113] from clinical samples, detection of virus, canine distemper virus [96], human herpesvirus, hu- DENV NS1 antigen from pools of mosquitoes [114] and man papillomaviruses, anelloviruses and circoviruses, genotyping of closely related Anopheles species [115]. among others [95]. One of the main limitations of xenosurveillance is the Conclusions difficulty in collecting sufficient blood engorged mosqui- Over the past decade, there have been key scientific ad- toes for analysis. Some of the methods to collect engorged vances in arbovirus surveillance, particularly with regard mosquitoes (i.e. use of an aspirator) are labour intensive to sample collection, virus detection and data analysis. and can be intrusive, especially when sampling inside Table 3 summarises the relative advantages and disadvan- houses and villages [99]. To circumvent this issue, mos- tages of current and emerging surveillance methodologies. quito excreta could be used to provide the template for Alternative samples for virus detection, such as mosquito xenosurveillance. Indeed, hepatitis B virus, which does not excreta, may enable more sensitive detection of arbovi- replicate in the vector, has been detected in mosquito ex- ruses than existing methodologies. It has been proposed creta by RT-PCR and Southern Blot up to 7 days after the that we are on the cusp of a revolution in genomic epi- ingestion of an infectious blood meal [100]. demiology [116]. With NGS technologies becoming more accessible in the near future, they will enable the collec- tion of real-time in-depth genetic information on circulat- Emerging technology ing arboviruses before or during an outbreak. There is still Integration of data acquisition, storage and sharing room for improvement of surveillance systems used in re- methodologies, such as cloud networks and geographic mote locations where surveillance coverage is limited by information systems, will form an integral component of cost and limited access to sites. Use of other sources of surveillance and control programmes. An example of CO in mosquito traps (such as fermentation using yeast) this is the Intelligent Dengue Monitoring technology [117]or CO -free systems could provide an alternative in (MI-Dengue) developed in Brazil [101]. MI-Dengue con- areas where dry ice or pressurized gas cylinders are not sists of an array of tools to collect gravid Ae. aegypti fe- available. Deployment of in-field portable molecular la- males, collect field data, detect virus and create boratories or point of care assays could provide same-day georeferenced infestation maps that are available in real assessment of arbovirus circulation and rapid response in time, providing information to optimize vector control. these locations [118]. In the future, other technologies, Ramírez et al. Parasites & Vectors (2018) 11:320 Page 8 of 12 Table 3 Summary of traditional and novel arbovirus surveillance methods Method Advantages Disadvantages Application Monitoring human and animal Uses data that is already being Overlap of clinical symptoms National disease surveillance disease collected by hospitals, health within arboviruses and other databases practitioners, and animal pathogens. Not ideal for early health personnel warning since active transmission will be already occurring Sentinel animals Can act as an early warning Animals can be amplifying Routine surveillance, inform system hosts. High costs associated control strategies with animal rearing. Cross reactivity between closely related arboviruses when using serological assays Virus isolation from pools of Increases virus titer allowing Time consuming. Requires Routine surveillance, virus mosquitoes for genotypic and phenotypic special infrastructure identification, inform control characterization (biological containment). strategies Requires a cold chain Virus detection in pools of Allows high throughput Will only detect RNA from Routine surveillance, research, mosquitoes using molecular screening. High sensitivity viruses that the assays were inform control strategies assays designed to detect. Requires special infrastructure Virus detection in pools of Rapid. Does not require Lower sensitivity than Routine surveillance in low mosquitoes using rapid specialized equipment. Lower molecular methods resource settings antigen detection assays cost Sugar-based surveillance Does not require a cold chain. Relies on a nanoliter amounts Routine surveillance, ideal for Only 1-2 samples per trap are of expectorate. Mosquitoes remote locations tested potentially compared need to be kept alive for as with 1000s of mosquitoes long as possible to increase using other methods of sur- feeding on cards. Cannot be veillance. Better estimation of used to incriminate mosquito transmission risk species as vectors. Requires special infrastructure Next-generation sequencing of Does not require prior High cost. Requires Research, virus discovery mosquito samples information (will detect any bioinformatics knowledge. arbovirus present in the Requires special infrastructure sample) Xenosurveillance Mosquito acts as an Blood engorged mosquitoes Research and surveillance of environmental sampler. Allows are difficult to collect arboviruses and other detection of viruses that do pathogens not replicate in the mosquito such as unmanned aerial vehicles (UAVs) could be used to Abbreviations DENV: Dengue virus; JEV: Japanese encephalitis virus; WNV: West Nile virus; automate sample collection in difficult to access locations CHIKV: Chikungunya virus; ZIKV: Zika virus; YFV: Yellow fever virus; SLEV: St. increasing the coverage of surveillance. Regardless of the Louis encephalitis virus; RRV: Ross River virus; BFV: Barmah Forest virus; surveillance system, there are always going to be issues MVEV: Murray Valley encephalitis virus; BTV: Blue tongue virus; RVFV: Rift Valley fever virus; EEEV: Eastern equine encephalitis virus; WEEV: Western and limitations, which can vary between jurisdictions. equine encephalitis virus; ISF: insect-specific flaviviruses; IgG: immunoglobulin Currently, the extent of arbovirus surveillance varies be- G; PCR: polymerase chain reaction; RT-PCR: reverse-transcription polymerase tween countries and even states with many jurisdictions chain reaction; RNA: ribonucleic acid; FTA®: Flinders Associate Technologies; PBT: passive box trap; SMACK: sentinel mosquito arbovirus capture kit; lacking any form of monitoring. There is a need for shar- C : cycle threshold; GAT: gravid Aedes trap; NGS: next-generation sequencing; ing of arbovirus surveillance intelligence between public UAV: unmanned aerial vehicle health agencies at regional level as a means to apply better control measures. Moreover, the implementation issues Acknowledgments that might arise from new approaches cannot be underes- The authors would like to acknowledge Brian J. Johnson and Kyran M. Staunton for their feedback on previous drafts of this article. timated. Agencies that are familiar with set methodologies may be reluctant to adopt new technologies or not have the capacity to implement change. Because of this, when Funding ALR was supported by a doctoral scholarship granted by the Australian designing new arbovirus surveillance methodologies, there Institute of Tropical Health and Medicine, James Cook University QLD, should be a clear understanding of the needs and limita- Australia. 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