Arbovirus vectors of epidemiological concern in the Americas: A scoping review of entomological studies on Zika, dengue and chikungunya virus vectors.

BACKGROUND: Three arthropod-borne viruses (arboviruses) causing human disease have been the focus of a large number of studies in the Americas since 2013 due to their global spread and epidemiological impacts: Zika, dengue, and chikungunya viruses. A large proportion of infections by these viruses are asymptomatic. However, all three viruses are associated with moderate to severe health consequences in a small proportion of cases. Two mosquito species, Aedes aegypti and Aedes albopictus, are among the world's most prominent arboviral vectors, and are known vectors for all three viruses in the Americas.
OBJECTIVES: This review summarizes the state of the entomological literature surrounding the mosquito vectors of Zika, dengue and chikungunya viruses and factors affecting virus transmission. The rationale of the review was to identify and characterize entomological studies that have been conducted in the Americas since the introduction of chikungunya virus in 2013, encompassing a period of arbovirus co-circulation, and guide future research based on identified knowledge gaps.
METHODS: The preliminary search for this review was conducted on PubMed (National Library of Health, Bethesda, MD, United States). The search included the terms 'zika' OR 'dengue' OR 'chikungunya' AND 'vector' OR 'Aedes aegypti' OR 'Aedes albopictus'. The search was conducted on March 1st of 2018, and included all studies since January 1st of 2013.
RESULTS: A total of 96 studies were included in the scoping review after initial screening and subsequent exclusion of out-of-scope studies, secondary data publications, and studies unavailable in English language. KEY
FINDINGS: We observed a steady increase in number of publications, from 2013 to 2018, with half of all studies published from January 2017 to March 2018. Interestingly, information on Zika virus vector species composition was abundant, but sparse on Zika virus transmission dynamics. Few studies examined natural infection rates of Zika virus, vertical transmission, or co-infection with other viruses. This is in contrast to the wealth of research available on natural infection and co-infection for dengue and chikungunya viruses, although vertical transmission research was sparse for all three viruses.

Introduction

Arboviruses, or arthropod-borne viruses, comprise a diverse group of viruses mostly transmitted by mosquitoes and ticks, including globally spreading viruses causing human disease, such as Zika, dengue, and chikungunya viruses. The term arbovirus does not encompass a taxonomically distinct group, but these viruses have similar life-history and transmission patterns that make information gleaned from one virus potentially useful to the understanding, and therefore prevention and control, of the others.

Since its identification in Uganda in 1947, Zika virus (Flavivirus, Flaviviridae) has been, until recently, confined only to Africa and Asia [1]. The virus ultimately reached the Americas in late 2014, resulting in the declaration of a Public Health Emergency of International Concern by the World Health Organization [2]. To date, 86 countries have reported evidence of mosquito-transmitted Zika virus infection. [3] Brazil currently faces the greatest burden of Zika virus infections [4]. Dengue fever, caused by four different serotypes of dengue virus (Flavivirus, Flaviviridae) is the most common arboviral disease that affects humans– 50 million people contract it each year, and an estimated 22,000 die from severe dengue [5]. Dengue is hyperendemic in the Americas, with cyclic epidemics occurring every three to five years [6]. Chikungunya virus (Alphavirus, Togoviridae) was first isolated in Tanzania in 1952 [7]. In the early 2000s, chikungunya virus cases and outbreaks were identified in countries in Africa, Asia, and Europe [7]. In 2013, it emerged in the Americas in Saint-Martin, and within the first year, over a million new cases were reported, spreading to 45 countries in the Latin American and Caribbean region [8].

A large proportion of Zika, dengue, and chikungunya viral infections are asymptomatic [9-11]. However, all three viruses are associated with moderate to severe health consequences in a small proportion of cases, with neonates, young children and/or older age groups at higher risk. Symptoms of Zika viral infection include rash, fever, arthralgia, and conjunctivitis [11]. More importantly, since its initial emergence in the Americas, Zika virus has been confirmed as a cause of congenital abnormalities (in infants born to women infected with Zika virus during pregnancy) and as a trigger of Guillain-Barré Syndrome [12]. Symptoms of dengue viral infection include rash, fever, arthralgia, and nausea. Some of the more severe symptoms of dengue viral infection may include deadly hemorrhage and plasma leak [9]. Symptoms of chikungunya viral infection include rash, fever, and arthralgia that may persist for an extended duration [7].

Two mosquito species, Aedes aegypti and Aedes albopictus, are among the world’s most prominent arboviral vectors. Ae. aegypti originated in sub-Saharan Africa as a sylvatic species and was introduced to the Americas via ships soon after European arrival in the 1400s [13]. The species became domesticated and is now endemic to the Americas and the Asia-Pacific. The range of Ae. albopictus was restricted to Asia until the latter part of the 20th century. It is thought to have been introduced to the Western hemisphere through a shipment of used tires in 1985 and has expanded its territory to over 40% of the world’s landmass over the course of the past 30 years [14-16].

This review summarizes the state of the literature surrounding the vectors of Zika, dengue and chikungunya viruses and factors affecting virus transmission in the Americas, with a focus on public health implications. Waddell et al. [17] conducted a comprehensive scoping review of the Zika virus literature in 2016. However, the authors identified a limited scope of literature on vector studies, and none specifically looked at vector populations of the Americas, highlighting the need for a scoping review focusing on this area given its relevance in understanding arboviral disease risk in the region. This scoping review aims to identify and characterize the literature pertaining to mosquito species vector competence and aspects of virus transmission dynamics in the Americas since the introduction of chikungunya in 2013. This timeframe includes the introduction of Zika virus and the ongoing co-circulation of three globally spreading arboviruses, namely Zika, dengue and chikungunya viruses.

Methods

This study’s search strategy and data extraction protocol were developed a priori. The list of definitions for each search term and the data characterization and utility form are available upon request. The review was conducted using PRISMA guidelines for scoping reviews [18]. See S2 Table for this scoping review’s checklist. The preliminary search for this review was conducted on PubMed (National Library of Health, Bethesda, MD, United States). The search included the terms ‘zika’ OR ‘dengue’ OR ‘chikungunya’ AND ‘vector’ OR ‘Aedes aegypti’ OR ‘Aedes albopictus’. The search was conducted on March 1st of 2018, and included all studies since January 1st of 2013. We chose the year 2013 as a start date for our search to reflect the timing of chikungunya virus spread to the Americas, followed in 2014 by Zika virus. These years are thus characterized by co-circulation of multiple globally spreading arboviruses in the region. Upon selection of potentially relevant articles, studies were characterized according to main characteristics including study setting, virus of interest, study design, methods of mosquito collection and analysis, vector species discussed, and main findings. Zotero (Center for History and New Media, George Mason University, United States) was initially used for title and abstract screening. All studies were subsequently transferred to Excel (Microsoft Corporation, Redmond, WA, United States) for data characterization and extraction. Two independent reviewers completed each step of the review following the broad initial screening, which was conducted by one reviewer.

Articles were selected if they were related to vector species composition and/or virus transmission dynamics, if they were related to Zika, dengue and/or chikungunya arboviruses, and if they were related to the ongoing virus circulation in the Americas. Other inclusion criteria included availability of an English language version and investigation of primary data. Studies that specifically examined the impacts of vector control measures, or studies that were unrelated to vector-borne aspects of disease, vector competence or entomological measures, were excluded due to the degree of scope expansion that would be caused by their inclusion.

Results

Descriptive statistics of scoping review

The search yielded 6267 results. All records were screened, and 5919 were not deemed relevant based on title and abstract content. A total of 348 screened full-text studies were examined for eligibility, and ultimately 96 studies were included in the scoping review (Fig 1; S1 Table). The vast majority of studies were performed exclusively in the field, in the laboratory, or using a modelling framework, and most studies were conducted exclusively on Ae. aegypti (Table 1). Studies focusing exclusively on dengue virus were the most numerous, followed by studies focusing exclusively on Zika virus, while studies focusing on chikungunya virus or on a combination of arboviruses were the least numerous (Table 1). Studies on virus transmission dynamics were the most numerous, while studies on aspects of both vector species composition and virus transmission dynamics were the least numerous (Table 1). The average monthly number of studies hovered between 0 and 2 from 2013 to 2016, then increased to 3 or more in 2017 and 2018 (Fig 2), closely reflecting the introductions of chikungunya and Zika viruses in the Americas and subsequent epidemics, respectively.

Fig 1

Summary of screening and exclusion steps of this scoping review’s methodology, and resulting number of publications after each step.

Table 1

Number of publications included in the scoping review, for each review section, study design, and arbovirus and mosquito vector species of interest.

Theme	Category	Number of publications
Section	Vector Species Composition	29
	Virus Transmission Dynamics	42
	Both sections	25
Study design	Field	16
	Laboratory	40
	Modelling	27
	Field and Laboratory	9
	Field and Modelling	3
	Laboratory and Modelling	1
Virus of interest	Zika	30
	Dengue	45
	Chikungunya	10
	Multiple	11
Mosquito species of interest	Ae. aegypti	52
	Ae. albopictus	6
	Cx. quinquefasciatus	3
	Ae. aegypti and Ae. albopictus	19
	Ae. aegypti and Cx. quinquefasciatus	1
	Ae. albopictus and Cx. quinquefasciatus	0
	Ae. aegypti, Ae. albopictus and Cx. quinquefasciatus	1
	Others	12
	None specifically	2

Fig 2

Average monthly number of publications included in the scoping review, for each year since 2013, out of a total of 96.

*Year-to-date on March 1st 2018.

Vector species composition

Zika virus

There is extensive evidence that Ae. aegypti mosquitoes are able to transmit Zika virus in both the laboratory [19-29] and in the field [30-32]. Ae. albopictus mosquitoes were also able to transmit Zika virus in experimental studies [22,23], but studies in which both Ae. aegypti and Ae. albopictus were captured found no Zika virus-infected Ae. albopictus [31,32]. Gendernalik et al. [33] and O’Donnell et al. [25] report that Ae. vexans mosquitoes are also experimentally competent vectors of Zika virus, but no studies indicated natural Ae. vexans infection with Zika virus. Cx. quinquefasciatus has been identified by predictive models as a potential vector for Zika virus [34], as have Sabethes and Haemagogus spp. [35]. Seven studies found that Cx. quinquefasciatus mosquitoes were refractory to Zika virus when exposed to infectious blood meals [29,36-42]. Ferreira-de-Brito et al. [31] reported that no Cx. quinquefasciatus captured in Brazil were positive for Zika virus. In contrast, Guedes et al. [43] detected Zika virus in the midgut, salivary glands and saliva of artificially fed Cx. quinquefasciatus captured in Brazil, using RT-PCR and transmission electron microscopy. The same study also reported Zika virus isolated from two field-caught Cx. quinquefasciatus in Brazil.

Dengue virus

Ae. albopictus [44-47] and Ae. aegypti [27,45,46,48-50] are both experimentally competent to transmit dengue virus. Infection by the virus is observed in field populations of Ae. albopictus [51-54], Ae. aegypti [51,52,54-62] and Cx. quinquefasciatus [56], although the latter was not identified as a competent vector species experimentally.

Chikungunya virus

Ae. aegypti [46,63-68], Ae. albopictus [46,64,66-69], Aedes terrens [70], and Haemagogus leucocelaenus [70] are all experimentally competent to transmit chikungunya virus. Chikungunya virus transmission in Ae. aegypti has also been observed in the field [30,59,71,72].

Virus transmission dynamics

Vector competence factors

Four studies measured the effect of temperature on vector competence [47,63,64,73]. Adelman et al. [63] found that under silenced RNAi conditions, Ae. aegypti were more predisposed to chikungunya infection at lower temperatures. Alto et al. [64] found that larger fluctuations in diurnal temperature range led to higher rates of chikungunya infection, and Xiao et al. [47] found that maximum dengue infection rates occurred at 31°C. Mordecai et al. [73] modelled Ae. aegypti and Ae. albopictus transmission in the Americas and found that mean temperature data accurately reflected Zika, chikungunya and dengue human case data. Transmission was found to occur between 18 and 34°C and maximal transmission was observed between 26–29°C, with less certainty surrounding the critical thermal minimum than the critical thermal maximum [73]. Ae. albopictus was found to perform better in cooler temperatures [73]. Buckner et al. [45] found that the interaction of low temperature and low food availability increased Ae. aegypti and Ae. albopictus susceptibility to DENV-1 serotype infection.

Three studies examined the effects of larval competition on dengue vector competence [44,45,74]. Bara et al. [44] found that Ae. albopictus larval competition resulted in significantly longer development times, lower emergence rates, and smaller adults, but did not significantly affect the extrinsic incubation period of DENV-2 virus. Kang et al. [74] found that larval-stage crowding and nutritional limitation led to lower survival rates until pupation, lower blood feeding success, slower development, smaller adult body size, and lower susceptibility to DENV-2 infection. Four studies examined a variety of blood meal characteristics on arboviral infection rate [23,24,49,75]. Fresh Zika-infected blood meal was associated with significantly higher infection rates than frozen Zika-infected blood meal [23]. Similarly, Zika-infected whole blood meal was associated with significantly higher infection rates than Zika-infected protein meal [24]. Hill et al. [49] studied the impact of antibiotics on dengue infection rate and mosquito fertility, and found no significant association in Ae. aegypti. Mosquitoes exposed to DENV-2 were more likely to re-feed than those that were unexposed [75]. Sylvestre et al. [76] studied the impact of DENV-2 infection on Ae. aegypti life history traits, and found that it significantly affected feeding behaviour, survival, fecundity, and oviposition success.

Vector infection rate

Two studies conducted in Brazil exclusively examined infection rates by Zika virus in wild mosquito populations (Table 2). Ferreira-de-Brito et al. [31] reported three Zika-infected pools of Ae. aegypti, but no Zika-infected Cx. quinquefasciatus or Ae. albopictus pool [31], out of 468 tested pools among the three species. Ayllón et al. [32] tested 406 Ae. aegypti and 11 Ae. albopictus field-collected individuals, and found three Zika-infected Ae. aegypti individuals.

Table 2

List of studies that report a proportion of positive mosquito pools for any or a combination of Zika, dengue and chikungunya viruses, along with information on authors, year and country of location of the study, and mosquito species of interest.

Authors	Year	Location	Mosquito species	Pools tested	Zika rate (%)	Dengue rate (%)	Chikungunya rate (%)
Ferreira-de-Brito et al.	2016	Brazil	Aedes sp. and Cx. quinquefasciatus	468	0.64	ø	ø
Ayllón et al.	2017	Brazil	Ae. aegypti and Ae. albopictus	178	1.12	ø	ø
Martínez et al.	2014	Mexico	Ae. aegypti	226	ø	0.88	ø
Calderón-Arguedas et al.	2015	Costa Rica	Ae. albopictus	35	ø	25.71	ø
Cecílio et al.	2015	Brazil	Aedes sp.	54	ø	7.41	ø
Cruz et al.	2015	Brazil	Ae. aegypti	50	ø	16.00	ø
Pérez-Castro et al.	2016	Colombia	Ae. aegypti	34	ø	61.76	ø
Pérez-Pérez et al.	2017	Colombia	Ae. aegypti and Ae. albopictus	407	ø	32.43	ø
Díaz-González et al.	2015	Mexico	Ae. aegypti	557	ø	ø	3.23
Cevallos et al.	2018	Ecuador	Ae. aegypti	22	14.29	ø	12.50
Dzul-Manzanilla et al.	2015	Mexico	Ae. aegypti	284	ø	9.51	3.17
Cigarroa-Toledo et al.	2016	Mexico	Ae. aegypti	27–237*	ø	0.00	0.84–7.40*
Farraudière et al.	2017	Martinique	Ae. aegypti	414	ø	1.21	2.66

*Total number of pools tested is not stated, but number of sampled mosquitoes, and maximum number of mosquitoes per pool, are stated.

Six studies reported exclusively on dengue infection rates in wild mosquito populations (Table 2). Cecílio et al. [77] observed four positive pools, out of 54 tested, among Aedes mosquitoes collected in two regions of Brazil over the course of 17 months, through the installation of ovitraps in public schools. Cruz et al. [57] detected eight positive pools, out of 50 Ae. aegypti pools, collected in Mato Grosso, Brazil. Martínez et al. [62] reported two positive pools, out of 226 Ae. aegypti pools, collected in Mexico. Claderón-Arguedas et al. [78] reported nine positive pools, out of 35 Ae. albopictus pools, collected in Costa Rica. Pérez-Pérez et al. [54] reported 132 positive pools, out of 407 tested, collected in Colombia. One of the positive pools was Ae. albopictus, and the remainder were Ae. aegypti. Pérez-Castro et al. [79] reported 21 positive pools, out of 34 tested, in Ae. aegypti in Colombia.

A study measured the naturally-occurring prevalence of chikungunya virus in wild mosquito populations (Table 2). Díaz-González et al. [72] reported 18 Ae. aegypti positive pools in Mexico, out of 557 tested. A study reported on the prevalence of both chikungunya and Zika viruses among Ae. aegypti in Ecuador (Table 2) [30]. Three studies tested both chikungunya and dengue viruses in wild mosquito populations (Table 2). Chikungunya, but not dengue, was detected in Ae. aegypti in Mexico by Cigarroa-Toledo et al. [71], although both chikungunya and dengue viruses were isolated in Mexico in Ae. aegypti by Dzul-Manzanilla et al. [59], and in Martinique by Farraudière et al. [61].

Vertical transmission

Three studies reported on vertical transmission of dengue virus [58,60,80], and one [81] reported on the vertical transmission of Zika virus. Buckner et al. [80] found a vertical transmission rate of DENV-1 of 11.11% in Ae. albopictus and of 8.33% in Ae. aegypti. Da Costa et al. [58] observed dengue infection rates among third and fourth instar Ae. aegypti between 1.14% and 2.41% in Brazilian municipalities, and Espinosa et al. [60] observed one DENV-3 positive male Ae. aegypti pool, collected in Argentina. Thangamani et al. [81] experimentally injected mosquitoes with Zika virus and observed Zika virus infection in Ae. aegypti offspring, but not Ae. albopictus. Six filial Ae. aegypti pools out of 69 tested were found positive for Zika virus [81].

Transmission risk modelling

Seven studies modelled transmission dynamics for Zika virus [40,82-87]. Lourenço et al. [40] used vectorial capacity as a means of prediction, Marini et al. [82] and Majumder et al. [83] used vector abundance and human case data, and Villela et al. [84] and Ospina et al. [85] used disease notification and natural history. Rojas et al. [86] found attack rates in Girardot and San Andres, Colombia to be highest among females, aged 20–49. Fitzgibbon et al. [87] report that early host and vector heterogeneity significantly affect final epidemic size.

Eleven studies modelled dengue transmission dynamics [88-99]. Lee et al. [95] constructed a predictive model that accurately foresaw 75% of dengue outbreaks in Colombia. Reiner et al. [88] reported that social proximity drives fine-scale heterogeneity in dengue transmission rates based on data from Peru. Three studies reported that meteorological variables including temperature and humidity are important determinants of transmission dynamics [89,90,92,93], and one study found that transovarial transmission plays an important role in transmission dynamics depending on basic reproductive number [91]. Liu-Helmersson et al. [96] predicted an increase in diurnal temperature range and increased dengue epidemic potential under climate changes in cold, temperate and extremely hot climates where mean temperatures are far from 29°C. Velasques-Castro et al. [97] studied Ae. aegypti dynamics in relation to host spatial heterogeneity and generated a dengue infection risk map, based on host dynamics. Taber et al. [98] modelled the colonization of Pennsylvania by Ae. albopictus together with corresponding risk of dengue.

One study estimated chikungunya transmission risk according to temperature threshold for breeding and adult mosquitoes in Argentina [99]. The authors suggest that temperatures conducive to Ae. aegypti breeding and transmission are present during September and April in northeastern Argentina, and in January in southern Argentina. A study compared endemic and transient chikungunya and dengue transmission dynamics, and the role of virus evolution [100]. They found that reducing biting rate and vector-to-susceptible-host ratio were the most effective at reducing basic reproductive number. A study modelled transmission risk of Zika, dengue and chikungunya and found temperature data to match well with human case data [73].

Strain infectivity and co-infection

Six studies examined the infectivity of different dengue viral strains, and the impact of co-infection [50,74,101-104]. Muturi et al. [50] found that infection with DENV-4 rendered Ae. aegypti significantly less susceptible to secondary infection with DENV-2. Kang et al. [74] modelled interactions between dengue viral serotypes. Quiner et al. [101] studied the infectivity of different isolates of DENV-2, and found NI-2B to have a replicative advantage over NI-1 until 12 days following infection, after which the advantage had dissipated. Quintero-Gil et al. [102] found that the DENV-2 serotype performed with a thousand-fold greater efficiency than the DENV-3 serotype, upon co-infection. In parallel, Serrato-Salas et al. [103] found that Ae. aegypti were significantly less susceptible to secondary dengue infection, after having been challenged with an inactive version of the virus. Vazeille et al. [104] found that DENV-4 outperformed DENV-1 in Ae. aegypti upon co-infection. Nuckols et al. [46] artificially infected Ae. aegypti and Ae. albopictus with chikungunya and DENV-2 simultaneously, separately, and in reverse order. Simultaneous dissemination was detected in all groups upon co-infection, and co-transmission occurred at low rates [46]. Rückert et al. [27] found that the co-infection of Ae. aegypti with Zika, chikungunya and dengue viruses minimally affected vector competence, and that vectors were able to transmit each viral pair, as well as three viruses simultaneously. Alto et al. [69] found Ae. aegypti and Ae. albopictus to be susceptible to Indian Ocean and Asian chikungunya virus genotypes.

Human disease risk

Five articles studied correlations between entomological measures and risk of human dengue infection [105-109]. One study conducted in Peru found that Ae. aegypti density was not associated with an increased risk of seroconversion [105]. One study in Acre, Brazil found that Ae. aegypti density and risk of dengue increased with tourism and case importation [106]. A study in Mexico City found a positive correlation between dengue incidence and Ae. aegypti indoor abundance, as well as monthly average temperature and rainfall [107]. Another study conducted in Peru found that an individual’s likelihood of being bitten in the home was directly proportional to time spent in the home, and body surface area. They did not find age or gender to be significant predictors [108]. Oliveira et al. [109] reported the circulation of four dengue serotypes in Brazil introduced between 2001 and 2012 (DENV-1, DENV-2, DENV-3, DENV-4) and reported an increase in dengue infection in Brazil during that time period, i.e. 587 cases/100 000 in 2001 to 1561 cases/100 000 in 2012. Monaghan et al. [110] predicted the seasonal abundance of Ae. aegypti in the United States using meterorologically driven models as a means of estimating arboviral infection risk [110]. All 50 included cities were found to be suitable during the summer months (July to September), while only cities in Florida and Texas were found to have Ae. aegypti abundance potential during the winter months (December to March). Lo and Park [111] found that regions of Brazil with elevated temperature and precipitation were more conducive to Ae. aegypti presence and Zika virus cases. Da Cruz Ferreira et al. [112] found that dengue occurrence increased by 25% when the average number of mosquitoes caught by traps increased by 0.1 per week. Stewart-Ibarra and Lowe [113] assessed the effect of climatic and entomological variables on intra-annual variability in dengue incidence in Southern Ecuador. Da Rocha Taranto et al. [114] examined the relationship between vector collection, species composition, hatching rates, and population density on dengue incidence. Hatching rate was found to be affected by population density and climate, and presence of vectors was associated with dengue incidence [114]. Ernst et al. [94] found no correlation between Ae. aegypti density and human age structure between two cities with different dengue transmission dynamics.

Discussion

Our scoping review included studies focused on vector species composition and arbovirus transmission dynamics of Zika, dengue and/or chikungunya in the Americas. We observed a steady increase in number of publications, from 2013 to 2018, with half of all studies published from January 2017 to March 2018. Sightly less than half of all studies included in this review were specifically pertaining to virus transmission dynamics. Around a third of all studies addressed vector species composition. The remainder treated aspects of both sections. Most studies focused on Aedes aegypti as the vector species of interest, had an exclusively laboratory-based or modelling-based study framework, and focused exclusively on either Zika or dengue. One limitation of our study is the use of a single search engine, PubMed, which may have reduced the number of included publications in our scoping review. However, given the focus of our scoping review, we believe this search engine should have captured almost all, if not all, relevant studies.

To determine vector competence, a species must be able to acquire, maintain, and transmit a pathogen, which is assessed through experimental infection studies. However, these studies are heterogeneous in both the mosquito populations and virus strains used, as well as methods measuring potential to transmit [115]. The detection of viral particles in wild-caught mosquitoes does not signify vector competence on its own, but it lends support to evidence from laboratory studies, when coupled with the observation of human host-feeding behaviour. Field studies are also important to assess the relative importance of competent vector species in disease maintenance and/or transmission. Vector competence for Zika virus has been well established for Ae. aegypti [19-32] and Ae. albopictus [22,23], but there is a growing consensus that Cx. quinquefasciatus is not a competent Zika virus vector, and no consensus has been reached regarding the competence of Ae vexans. A number of studies report that Cx. quinquefasciatus is refractory to Zika virus [29,36-39,41,116]. While Zika virus has been detected in a small number of field-caught Cx. quinquefasciatus in Brazil [42], this does not necessarily indicate their ability to transmit the virus. Interestingly, information on Zika virus vector species composition was abundant, but sparse on Zika virus transmission dynamics. Few studies examined natural infection rates of Zika virus [31,32], vertical transmission [81], or co-infection with other viruses [27]. This is in contrast to the wealth of research available on natural infection and co-infection for dengue and chikungunya viruses, although vertical transmission research was sparse for all three viruses [46,50,58,77,80,101,102].

Based on the internationally recognized urgency of Zika virus infection as a public health concern, and potential increase in the importance of this and other emerging arboviruses in the future, further research on Zika virus transmission dynamics is of pressing need. Also, given the ongoing co-circulation of these three globally spreading arboviruses in the Americas, and the resulting complexity of their transmission dynamics, more integrative studies are needed that investigate a combination of Zika, dengue and chikungunya viruses and use a variety of approaches to answer questions relating to the risk posed by these arboviruses.

List of full-text articles included in the review.

Information on first author’s last name, year of publication, title, journal, review section, study design, and arbovirus and mosquito vector species of interest are given for each full-text article.

(XLSX)

Click here for additional data file.

PRISMA-ScR checklist.

Checklist stating location of each element of the scoping review, as implemented by Tricco et al. [18].

(PDF)

Click here for additional data file.

4 Oct 2019

PONE-D-19-19188

Arbovirus Vectors of Epidemiological Concern in the Americas: A Scoping Review of Entomological Studies on Zika, Dengue and Chikungunya Virus Vectors

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Additional Editor Comments:

I invited and received two reviews of your manuscript; both reviews raised some substantial concerns for your manuscript as it currently stands. I completely agree to the point raised by reviewers that your study missed many literature including ones that we published later (#check Samy et al. 2016). Please respond properly for all comments raised by our reviewers below. I would kindly ask you to check the Journal style requirements before submitting a revised version of your manuscript.

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Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #1: N/A

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #2: Yes

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Reviewer #1: The manuscript is a scoping review that provides an overview on the current state of entomological knowledge of the mosquito vectors of Zika, dengue and chikungunya viruses in the Americas. The authors performed a thorough review of articles on these viruses and theirs hosts published between January 2013 and March 2018. I believe that this study represents a valuable overview of a wide body of research. However, I believe that the study does not entirely meet its own objectives, and could benefit from a more focused approach and a bit more synthesis. I am also concerned that the short time-frame examined by the authors does not provide a full and accurate picture of the literature on several topics. While the nature of publishing makes it impossible for a review to capture all of the most up-to-date papers, the time frame set by the authors starts too late to capture many valuable studies on important vector species. The authors’ time frame seems suited to a study of public health effects of these arboviruses in the Americas, but there is much more entomological literature from the ‘90s and 2000s that would provide a much more complete picture on this subject. I would strongly encourage the authors to broaden their time frame.

A few comments and suggestions are listed below:

Abstract:

1) Line 28: Please correct the spelling of “arthropod”

2) Line 34: I don’t know that I agree with this. While Ae. albopictus has demonstrated vector competence for all three viruses, and has been implicated in the transmission of these viruses in Europe, Asia and the Americas, there is still little evidence that it is the primary vector for any of these viruses in the Americas. Please remove the word “primary”.

3) Line 49: This seems like a bit of a leap, given that the authors list several good studies on interspecific competition. Perhaps it would be better to say simply that much work is left to be done regarding interspecific competition, given the breadth of the topic.

4) General comments: I would like to see some mention of methods in the abstract. Also, it seems redundant to have both “Key findings” and “Conclusions,” especially given how short the “Conclusions” section is.

Introduction:

5) Lines 61-63: This language is somewhat confusing. It implies that ZIKV, DENV and CHIKV are the only arboviruses with global health implications. It also makes it somewhat unclear that "arboviruses" and "arthropod-borne viruses" are the same thing.

6) Line 68: What is the meaning of “uncharacterized” here? Perhaps it would be better to say that until recently ZIKV transmission has been confined to Africa and Asia.

7) Line 93: Arthralgia can actually persist for over a year, if not longer. See Gianandrea et al., 2008.

8) Line 109: I’m not sure about the term “evidence” here. Perhaps “knowledge” would be more accurate?

Methods:

9) Lines 117-118: I would suggest that the authors consider using an additional search library, such as Web of Science. It might provide a broader pool of results.

10) General comment: Was this study conducted using PRISMA guidelines? If so, please mention this and provide PRISMA checklist.

Results:

11) Lines 200-205: This section is a prime example of why this paper could benefit from broadening the examined time frame. There are papers from Richards et al. (2006), Dennett et al. (2007), and Niebylski et al. (1994) that provide a much more complete picture of Ae. albopictus blood feeding behavior in North America.

12) Lines 293-299: Medley et al. (2014) also provides valuable insight into Ae. albopictus population genetics across North America. Not sure why this did not meet study criteria.

Discussion:

13) Line 103: Please replace “immatures” with a more correct term. “immature stages” or “larvae” would be fine.

14) Line 108: “have been consistently with arbovirus vector occurrence”… Consistently associated? Please clarify.

15) Line 111: Again, I do not think it is fair to say that it is poorly understood, though more research is certainly needed. Please rephrase.

General overall comments:

16) Please review manuscript for spelling errors and punctuation.

17) While the manuscript lays out much of the research around ZIKV, DENV, CHIKV and vector species, it does not provide much in the way of highlighting knowledge gaps. I think this would be a much stronger paper if there were more emphasis in the discussion on specifically highlighting issues that need more research to resolve.

Reviewer #2: In this manuscript the authors provide a review of entomological studies of three emerging arboviruses of critical concern in the past decade. Though this sort of review has been conducted before, this manuscript distinguishes itself by providing a framework for identifying knowledge gaps and guiding future research.

This scoping review is certainly informative, but it reads more as a perspective piece than a research article. While there is nothing wrong with that, it should be clearer in its presentation of that fact.

Even in a scoping review article, I believe a manuscript should still address key questions and I felt that this review read more as a book chapter than a research article. While the authors do include the question “What is the current state of the evidence on mosquito vector population dynamics and behaviour, mosquito vector distribution and environmental suitability, vector species composition and virus transmission by mosquito vectors as they relate to Zika, dengue

and chikungunya viruses in the Americas?” this is a very broad overarching inquiry. I would have preferred specific directed questions which are supported by the scoping review. For example, Are Ae. aegypti and Ae. albopictus distributions influenced by specific environmental conditions? Is this uniform globally? As a scoping review which aims to highlight knowledge gaps I felt that this kind of structure would be beneficial.

I would have liked to see more directed questions.

Abstract

-arthropod is misspelled

-Why were only studies from 2013 considered? Because of the shift in focus to research on these viruses? What about studies between 2013 and 2016 which were covered in Waddell et al.

-How much overlap is there between the 2016 scoping review and this one?

LN 62: yes largely, but new findings highlight the importance of ticks and other arthropods, otherwise we could call them mosquito-borne viruses. Please modify to specify that many are transmitted by mosquitoes instead of largely.

LN 93: background information on chikungunya seems pale in comparison to that of Zika and dengue. Since this is not just a scoping review of Zika, I would expand the section on chikungunya significantly

Ln 95: sub-Saharan Africa

LN 101: please include

Kraemer, M.U., Reiner, R.C., Brady, O.J., Messina, J.P., Gilbert, M., Pigott, D.M., Yi, D., Johnson, K., Earl, L., Marczak, L.B. and Shirude, S., 2019. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nature microbiology, 4(5), p.854.

While the statement in LN 205: “Vinauger et al. [29] experimentally demonstrated the importance of dopamine in relation to host-seeking behaviour” is interesting, this falls more within behavior than blood feeding. Host seeking and feeding are different strategies and dopamine being an attractant may not influence patterns of blood feeding unless you have species differences in the release of dopamine.

LN 154: chikungunya should be lower case

LN 200: No comment is made about Culex

The subsections of the results are intriguing, but I find that some sections are lacking in content beyond one or two studies.

LN 334: there have been conflicting studies on socioeconomics and Aedes vectors and geography

This review provides a long list of directions in which future researchers can begin to investigate and this review is well outlines and compiled; however, all of the outstanding questions seem scattered throughout the text. I would prefer to see a conceptual figure outlining the different disciplines and specific questions remaining. If not a figure, a table would be a very useful guide or framework for researchers to build off of.

**********

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Reviewer #1: No

Reviewer #2: No

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15 Nov 2019

Here you can find the list of comments from the editor and two reviewers, in black font, with our response indented below each. The respective changes are highlighted in the edited manuscript file.

Additional Editor Comments:

I invited and received two reviews of your manuscript; both reviews raised some substantial concerns for your manuscript as it currently stands. I completely agree to the point raised by reviewers that your study missed many literature including ones that we published later (#check Samy et al. 2016). Please respond properly for all comments raised by our reviewers below. I would kindly ask you to check the Journal style requirements before submitting a revised version of your manuscript.

We thank the editor for their suggestion of an additional publication that seems to be missing from our reference list. However, it is important to point out that our inclusion criteria specified studies that analyzed some primary data. It seems the suggested reference solely analyzes secondary data. According to comments of the two reviewers, we decided to adopt a more focused approach to frame our scoping review. We modified a sentence at lines 8-10 of page 6 to reflect this.

Reviewers' comments:

Reviewer #1: The manuscript is a scoping review that provides an overview on the current state of entomological knowledge of the mosquito vectors of Zika, dengue and chikungunya viruses in the Americas. The authors performed a thorough review of articles on these viruses and theirs hosts published between January 2013 and March 2018. I believe that this study represents a valuable overview of a wide body of research. However, I believe that the study does not entirely meet its own objectives, and could benefit from a more focused approach and a bit more synthesis. I am also concerned that the short time-frame examined by the authors does not provide a full and accurate picture of the literature on several topics. While the nature of publishing makes it impossible for a review to capture all of the most up-to-date papers, the time frame set by the authors starts too late to capture many valuable studies on important vector species. The authors’ time frame seems suited to a study of public health effects of these arboviruses in the Americas, but there is much more entomological literature from the ‘90s and 2000s that would provide a much more complete picture on this subject. I would strongly encourage the authors to broaden their time frame.

We thank the reviewer for their useful suggestions. We agree that the timeframe of the review does not capture many earlier studies in the entomological literature pertaining to arbovirus vectors, and have therefore reframed our scoping review’s questions to focus more specifically on identifying and characterizing the literature related to vector species composition and arbovirus transmission dynamics in a region of recent arbovirus introduction and ongoing co-circulation. This justification for including studies from 2013 is now stated in the Introduction on lines 5-9 of page 5.

A few comments and suggestions are listed below:

Abstract:

1) Line 28: Please correct the spelling of “arthropod”

We fixed the word in question.

2) Line 34: I don’t know that I agree with this. While Ae. albopictus has demonstrated vector competence for all three viruses, and has been implicated in the transmission of these viruses in Europe, Asia and the Americas, there is still little evidence that it is the primary vector for any of these viruses in the Americas. Please remove the word “primary”.

We fixed the sentence in question, and removed the word “primary” from it.

3) Line 49: This seems like a bit of a leap, given that the authors list several good studies on interspecific competition. Perhaps it would be better to say simply that much work is left to be done regarding interspecific competition, given the breadth of the topic.

We fixed the sentence in question.

4) General comments: I would like to see some mention of methods in the abstract. Also, it seems redundant to have both “Key findings” and “Conclusions,” especially given how short the “Conclusions” section is.

Introduction:

We merged the abstract sections “Key findings” and “Conclusions” into a section named “Key findings”. We also added a “Methods” abstract section.

5) Lines 61-63: This language is somewhat confusing. It implies that ZIKV, DENV and CHIKV are the only arboviruses with global health implications. It also makes it somewhat unclear that "arboviruses" and "arthropod-borne viruses" are the same thing.

We fixed the sentence in question.

6) Line 68: What is the meaning of “uncharacterized” here? Perhaps it would be better to say that until recently ZIKV transmission has been confined to Africa and Asia.

We fixed the sentence in question.

7) Line 93: Arthralgia can actually persist for over a year, if not longer. See Gianandrea et al., 2008.

We fixed the sentence in question.

8) Line 109: I’m not sure about the term “evidence” here. Perhaps “knowledge” would be more accurate?

We fixed the sentence in question.

Methods:

9) Lines 117-118: I would suggest that the authors consider using an additional search library, such as Web of Science. It might provide a broader pool of results.

We thank the reviewer for their suggestion. We have reframed the review to focus more closely on vector species composition and arbovirus transmission dynamics with implications for public health, and as such we feel that the Pubmed search engine is suitable to identify relevant primary literature for our scoping review. Our search terms and inclusion criteria were intentionally broad to capture a wide range of studies. However, we have mentioned this as a limitation in the discussion, at lines 5-9 of page 17.

10) General comment: Was this study conducted using PRISMA guidelines? If so, please mention this and provide PRISMA checklist.

We added a sentence to state that we used PRISMA guidelines, at lines 14-15 of page 5.

Results:

11) Lines 200-205: This section is a prime example of why this paper could benefit from broadening the examined time frame. There are papers from Richards et al. (2006), Dennett et al. (2007), and Niebylski et al. (1994) that provide a much more complete picture of Ae. albopictus blood feeding behavior in North America.

According to a previous comment by the reviewer, we adopted a more focused approach for our scoping review. With this new focus, we decided to remove the review section in question.

12) Lines 293-299: Medley et al. (2014) also provides valuable insight into Ae. albopictus population genetics across North America. Not sure why this did not meet study criteria.

According to a previous comment by the reviewer, we adopted a more focused approach for our scoping review. With this new focus, we decided to remove the review section in question.

Discussion:

13) Line 103: Please replace “immatures” with a more correct term. “immature stages” or “larvae” would be fine.

We fixed the sentence in question.

14) Line 108: “have been consistently with arbovirus vector occurrence”… Consistently associated? Please clarify.

We fixed the sentence in question.

15) Line 111: Again, I do not think it is fair to say that it is poorly understood, though more research is certainly needed. Please rephrase.

We removed the sentence in question.

General overall comments:

16) Please review manuscript for spelling errors and punctuation.

We made a thorough spelling and punctuation check of the entire manuscript..

17) While the manuscript lays out much of the research around ZIKV, DENV, CHIKV and vector species, it does not provide much in the way of highlighting knowledge gaps. I think this would be a much stronger paper if there were more emphasis in the discussion on specifically highlighting issues that need more research to resolve.

According to a previous comment by the reviewer, we adopted a more focused approach for our scoping review. We reframed the discussion to reflect these changes and added more focus to highlight knowledge gaps.

Reviewer #2: In this manuscript the authors provide a review of entomological studies of three emerging arboviruses of critical concern in the past decade. Though this sort of review has been conducted before, this manuscript distinguishes itself by providing a framework for identifying knowledge gaps and guiding future research.

This scoping review is certainly informative, but it reads more as a perspective piece than a research article. While there is nothing wrong with that, it should be clearer in its presentation of that fact.

Even in a scoping review article, I believe a manuscript should still address key questions and I felt that this review read more as a book chapter than a research article. While the authors do include the question “What is the current state of the evidence on mosquito vector population dynamics and behaviour, mosquito vector distribution and environmental suitability, vector species composition and virus transmission by mosquito vectors as they relate to Zika, dengue

and chikungunya viruses in the Americas?” this is a very broad overarching inquiry. I would have preferred specific directed questions which are supported by the scoping review. For example, Are Ae. aegypti and Ae. albopictus distributions influenced by specific environmental conditions? Is this uniform globally? As a scoping review which aims to highlight knowledge gaps I felt that this kind of structure would be beneficial.

I would have liked to see more directed questions.

We thank the reviewer for their suggestion. According to a comment by another reviewer and also this comment by the reviewer, we have reframed our scoping review’s questions to focus more specifically on identifying and characterizing the literature related to vector species composition and arbovirus transmission dynamics in a region of recent arbovirus introduction and ongoing co-circulation. This justification for including studies from 2013 is now stated in the Introduction on lines 5-9 of page 5.

Abstract

-arthropod is misspelled

We fixed the word in question.

-Why were only studies from 2013 considered? Because of the shift in focus to research on these viruses? What about studies between 2013 and 2016 which were covered in Waddell et al.

-How much overlap is there between the 2016 scoping review and this one?

According to a comment by another reviewer and this comment by the reviewer, we have reframed our scoping review’s questions to focus more specifically on identifying and characterizing the literature related to vector species composition and arbovirus transmission dynamics in a region of recent arbovirus introduction and ongoing co-circulation. This justification for including studies from 2013 is now stated in the Introduction on lines 5-9 of page 5.

Also, it is important to point out that no study about vector species composition and virus transmission dynamics included in Waddell et al.’s paper was specifically related to ongoing circulation in the Americas, which was one of our selection criteria. Therefore, there is no overlap of studies between our scoping review and Waddell et al.’s. We modified a sentence at lines 1-5 of page 5 to state this.

LN 62: yes largely, but new findings highlight the importance of ticks and other arthropods, otherwise we could call them mosquito-borne viruses. Please modify to specify that many are transmitted by mosquitoes instead of largely.

We fixed the sentence in question.

LN 93: background information on chikungunya seems pale in comparison to that of Zika and dengue. Since this is not just a scoping review of Zika, I would expand the section on chikungunya significantly

We acknowledge the section on Zika virus is much lengthier than the section on dengue and chikungunya viruses. We decided to remove some of the context information about Zika which is not directly important to set our scoping review in context. The extent of background information for all three arboviruses is now similar.

Ln 95: sub-Saharan Africa

We fixed the word in question.

LN 101: please include

Kraemer, M.U., Reiner, R.C., Brady, O.J., Messina, J.P., Gilbert, M., Pigott, D.M., Yi, D., Johnson, K., Earl, L., Marczak, L.B. and Shirude, S., 2019. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nature microbiology, 4(5), p.854.

We included the specific reference in the sentence in question.

While the statement in LN 205: “Vinauger et al. [29] experimentally demonstrated the importance of dopamine in relation to host-seeking behaviour” is interesting, this falls more within behavior than blood feeding. Host seeking and feeding are different strategies and dopamine being an attractant may not influence patterns of blood feeding unless you have species differences in the release of dopamine.

According to a previous comment by the reviewer, we adopted a more focused approach for our scoping review. With this new focus, we decided to remove the review section in question.

LN 154: chikungunya should be lower case

We fixed the word in question.

LN 200: No comment is made about Culex

The subsections of the results are intriguing, but I find that some sections are lacking in content beyond one or two studies.

LN 334: there have been conflicting studies on socioeconomics and Aedes vectors and geography

According to a previous comment by the reviewer, we adopted a more focused approach for our scoping review. With this new focus, we decided to remove the review sections in question.

7 Jan 2020

Arbovirus Vectors of Epidemiological Concern in the Americas: A Scoping Review of Entomological Studies on Zika, Dengue and Chikungunya Virus Vectors

PONE-D-19-19188R1

Dear Dr. Talbot,

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Academic Editor

PLOS ONE

23 Jan 2020

PONE-D-19-19188R1

Arbovirus Vectors of Epidemiological Concern in the Americas: A Scoping Review of Entomological Studies on Zika, Dengue and Chikungunya Virus Vectors

Dear Dr. Talbot:

I am pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

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