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Comparative analysis of the susceptibility of Aedes aegypti and Japanese Aedes albopictus to all dengue virus serotypes

Tropical Medicine and Health volume 51, Article number: 61 (2023) Cite this article

Abstract

Background

Dengue fever, caused by the dengue virus (DENV), is the most common viral infection transmitted by Aedes mosquitoes (mainly Ae. aegypti and Ae. albopictus) worldwide. Aedes aegypti is not currently established in Japan, and Ae. albopictus is the primary vector mosquito for DENV in the country, but knowledge of its viral susceptibility is limited. Therefore, we aimed to clarify the status of DENV susceptibility by comparing the infection and dissemination dynamics of Japanese Ae. albopictus to all known DENV serotypes with those of Ae. aegypti.

Methods

After propagation of each DENV serotype in Vero cells, the culture supernatants were mixed with defibrinated rabbit blood and adenosine triphosphate, and the mixture was artificially blood-sucked by two colonies of Ae. albopictus from Japan and one colony of Ae. aegypti from a dengue-endemic country (Vietnam). After 14 days of sucking, the mosquito body was divided into two parts (thorax/abdomen and head/wings/legs) and total RNA was extracted from each sample. DENV RNA was detected in these extracted RNA samples using a quantitative RT-PCR method specific for each DENV serotype, and infection and dissemination rates were analyzed.

Results

The Japanese Ae. albopictus colonies were susceptible to all DENV serotypes. Its infection and dissemination rates were significantly lower than those of Ae. aegypti. However, the number of DENV RNA copies in Ae. albopictus was almost not significantly different from that in Ae. aegypti. Furthermore, Japanese Ae. albopictus differed widely in their susceptibility to each DENV serotype.

Conclusions

In Japanese Ae. albopictus, once DENV overcame the midgut infection barrier, the efficiency of subsequent propagation and dissemination of the virus in the mosquito body was comparable to that of Ae. aegypti. Based on the results of this study and previous dengue outbreak trends, Ae. albopictus is predicted to be highly compatible with DENV-1, suggesting that this serotype poses a high risk for future epidemics in Japan.

Background

Dengue fever, caused by infection with dengue virus (DENV), is mainly endemic to tropical and subtropical regions of the world and is the most common mosquito-borne viral infection [1]. There are four serotypes of DENV (DENV-1, DENV-2, DENV-3, and DENV-4). A heteroserotype DENV secondary infection (different serotype from the primary infection) is the greatest risk factor for severe dengue, which can lead to organ failure and death [2]. DENV is maintained in nature through transmission between mosquitoes and vertebrates, including humans. In urban area, DENV is transmitted between urban Aedes mosquitoes (Aedes aegypti and Ae. albopictus) and humans [3]. Of the two vector species involved in the urban cycle of DENV transmission, the Ae. aegypti mosquito is considered the primary vector [4]. This is thought to be due to the higher vectorial capacity of DENV and the unique ecology of the species (high blood-sucking preference for humans, living in human dwellings, etc.), which increases the efficiency of DENV transmission [4]. In contrast, Ae. albopictus prefers vegetated environments and typically suck blood from various animals, including humans [5,6,7]. The distribution of Ae. albopictus is wider than that of Ae. aegypti, ranging from tropical to temperate regions. Therefore, in temperate regions where Ae. aegypti is absent, Ae. albopictus is the main vector of DENV. Outbreaks in which this species was the sole vector have recently been reported in several temperate regions worldwide (Table 1). Even in tropical and subtropical regions, there are areas where Ae. albopictus is the dominant species, and relatively large dengue epidemics have also been reported from the US state of Hawaii and China [8,9,10]. Thus, these cases demonstrate the potential of Ae. albopictus to spread DENV at the same level as the main vector mosquito, Ae. aegypti.

Table 1 Autochthonous transmission of dengue virus by Aedes albopictus mosquitoes in the temperate zone from 2010 to 2022
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Much of Japan’s land area lies in a temperate zone, and Ae. aegypti is not currently established in the country [11]. Several autochthonous outbreaks of dengue have been reported in Japan, but imported cases typically initiate every epidemic as the virus is not native to the country [12]. The most recent large dengue outbreak in Japan occurred in Tokyo in 2014 [13]. During this outbreak, the virus was transmitted by Ae. albopictus [13,14,15]. This outbreak ultimately resulted in 162 reported cases [15], the highest number of cases reported in recent dengue outbreaks in temperate regions (Table 1). Additionally, cases of other autochthonous dengue infections were reported also in 2019 [16]. Furthermore, approximately over 70 years prior to these outbreaks, during World War II, Japan experienced a large-scale domestic dengue epidemic, and Ae. albopictus was the main vector at that time (reviewed by Kurihara [17]).

Several fragmentary studies have investigated the susceptibility and vectorial capacity of Japanese Ae. albopictus to DENVs [18,19,20,21,22]. However, no study has compared the susceptibility of Japanese Ae. albopictus to all DENV serotypes using the same mosquito strain or colony, nor compared it with that of Ae. aegypti. Therefore, we aimed to clarify the status of DENV susceptibility in a unified manner by comparing the infection and dissemination dynamics of Japanese Ae. albopictus to all DENV serotypes with those of Ae. aegypti.

Methods

Mosquito colonies

Two colonies of Japanese Ae. albopictus were used in this study. The colony named IKT was derived from individuals collected in Kawasaki City, Kanagawa Prefecture (Japan) in 2008 (Table 2) [20]. The colony was subsequently reared in the laboratory for more than 50 generations since field collection. This colony was found to be susceptible to DENV-1 and DENV-2 in a previous study [20]. The other Ae. albopictus colony used in this study was individuals of the third generation since collection in Numata City, Gumma Prefecture, Japan (colony name BSD; Table 2). Because of the possibility that foreign Ae. albopictus populations are collected near ports and international airports [23, 24], we used Ae. albopictus collected in Numata City (inland and without nearby airports). In addition, Ae. aegypti mosquitoes collected in Ho Chi Minh City, Vietnam, a dengue-endemic area, were used as positive controls (designated HCM; Table 2) [25]. These mosquito colonies were fed a ground diet (Oriental Yeast Industry, Tokyo, Japan) during the larval stage, and adults reared on a 3% sucrose solution. Females were fed mouse blood and allowed to lay eggs. Both larvae and adults were reared at 25 °C and 70% humidity with a 16 h light (L):8 h dark (D) cycle.

Table 2 Mosquito colonies used in this study
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Dengue viruses

DENV strains obtained during the autochthonous outbreak [26] or derived from imported cases [27, 28] were used in all experiments (Table 3). Each virus was propagated in Vero cells (derived from African green monkeys; Department of Veterinary Science, National Institute of Infectious Diseases, Japan) before the experiment. Viral titers were determined by a focus-forming assay using the same method as described in a previous study [25].

Table 3 Dengue viruses used in this study
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Infection experiment

Infection experiments were performed similarly to those described in our previous studies [25, 29]. Briefly, a mixture of the culture supernatant containing DENV, rabbit defibrinated blood (Nippon Biotest Laboratories. Inc., Tokyo, Japan), and adenosine triphosphate (final concentration, 3 mM) (Fujifilm Wako Pure Chemical, Osaka, Japan) was prepared, and artificial blood-sucking performed using the Hemotek 5W1 membrane feeding system for blood-sucking insects (Hemotek Ltd., Blackburn, UK). Adult females within 10 days after emergence that had fasted overnight were allowed to feed on blood for 1 h. Only fully fed individuals were sorted under a stereomicroscope and used in subsequent experiments. Engorged mosquitoes were kept in a cage containing a 3% sucrose solution at 28 °C with a 16L:8D cycle. To facilitate normal physiology and metabolism, an oviposition tray was placed in the cage on which the mosquitoes were allowed to lay eggs. Under these conditions, the mosquitoes were maintained for 14 days after blood-feeding.

Quantitative measurement of dengue virus RNA in mosquito body parts

To measure the dynamics of DENV propagation in mosquitoes, the copy number of DENV RNA in different body parts of individuals was determined using quantitative RT-PCR, as previously described [25, 29]. Briefly, individual mosquitoes were anesthetized with CO2 14 days after feeding on DENV-containing blood, and the head, wings, and legs separated from the thorax and abdomen under a microscope. Total RNA was extracted from samples using NucleoSpin RNA (Takara Bio, Shiga, Japan). TaqMan Fast Virus 1-Step Master Mix for qPCR (Thermo Fishier Scientific, Waltham, MA USA) was then used to measure the copy number of DENV RNA using the QuantStudio 1 real-time PCR system (Thermo Fishier Scientific). Standard RNAs for each DENV serotype used in this experiment were synthesized in the same manner as previously described [25, 29]. The primer sets and probes used for quantitative RT-PCR, as well as primers used for standard RNA synthesis, are listed in Additional file 1.

In this study, the DENV infection rate (IR) and dissemination rate (DR) were calculated using the following formulae:

$${\text{IR}} = {\text{Number}}\,{\text{of}}\,{\text{individuals}}\,{\text{with}}\,{\text{DENVRN}}\,{\text{A}}\,{\text{detected}}\,{\text{in}}\,{\text{the}}\,{\text{thorax}}\,{\text{and}}\,{\text{abdomen}}/{\text{total}}\,{\text{number}}\,{\text{of}}\,{\text{individuals}}\,{\text{tested}} \times 100.$$
$${\text{DR}} = {\text{Number}}\,{\text{of}}\,{\text{individuals}}\,{\text{with}}\,{\text{DENVRN}}\,{\text{A}}\,{\text{detected}}\,{\text{in}}\,{\text{the}}\,{\text{head}},{\text{wings}},\,{\text{and}}\,{\text{legs}}/{\text{total}}\,{\text{number}}\,{\text{of}}\,{\text{individuals}}\,{\text{tested}} \times 100.$$

Statistical analyses

Data from the experiments were analyzed using R and GraphPad Prism software (GraphPad Software Inc., San Diego, CA, USA), as well as the Statistics calculators (http://www.statskingdom.com).

Results

Artificial blood-feeding and dengue virus infection status in each mosquito colony

DENV propagated in Vero cells resulted in titers of 0.72–7.17 × 106 focus forming units (FFU)/mL in the blood fed on by mosquitoes (Table 3). In the infection experiments, 40 to 50 mosquitoes were obtained in each experimental group 14 days after blood-feeding (Table 4).

Table 4 Summary of dengue virus (DENV) infection and dissemination status in mosquito colonies
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The IR of all DENV serotypes was significantly higher in the Ae. aegypti HCM colony than in both Ae. albopictus colonies (Fig. 1A, Table 4). There were differences in the IR between Ae. albopictus colonies, with the DENV-1 IR being significantly higher in the BSD colony than in the IKT colony (Fig. 1A, Table 4). The greatest difference in the IR was observed for DENV-3, where the Ae. aegypti HCM colony had a 12-fold higher IR than that of the Ae. albopictus IKT colony (Table 4).

Fig. 1
figure 1

Comparison of the infection and dissemination rates of dengue viruses between mosquito species and colonies. Bars indicate the infection (A) and dissemination rates (B) at 14 days post-infection with dengue virus (DENV) serotypes in the Aedes aegypti (Aae) HCM and Ae. albopictus (Aal) IKT and BSD colonies. Error bars represent 95% confidence intervals. Statistical analyses were performed using Fisher's exact test with Bonferroni correction. **, P < 0.0001; *, P < 0.001; ns, no significant differences (P > 0.01)

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Although significant differences in IR were observed between species and colonies, only the Ae. aegypti HCM colony had a significantly higher DENV-3 RNA copy number than that of the Ae. albopictus BSD colony in the thorax and abdomen; otherwise, there were no significant differences in the DENV RNA copy number between species or colonies (Fig. 2A).

Fig. 2
figure 2

Comparison of dengue virus RNA copy numbers in Aedes aegypti and Japanese Ae. albopictus colonies. Plots showing the copy numbers of dengue virus (DENV) RNA in the thorax and abdomen (A) and the head, wings, and legs (B) of individual mosquitoes of the Aedes aegypti (Aae) HCM and Ae. albopictus (Aal) IKT and BSD colonies 14 days after infection with each DENV serotype. Bars represent the mean with a 95% confidence interval. Statistical analyses were performed using the Mann–Whitney U test with Bonferroni correction. **, P < 0.0001; *, P < 0.001; ns, no significant differences (P > 0.01)

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IRs between different serotypes in the same mosquito colony were also compared (Additional file 2). The IR appeared to be influenced by differences in viral titers in the bloodmeal used for the infection experiment (Table 2), but values tended to vary widely between mosquito colonies. Among the DENV serotypes, the highest IRs were observed for DENV-1 in Ae. aegypti HCM and Ae. albopictus BSD colonies and for DENV-4 in the Ae. albopictus IKT colony (Table 4, Additional file 2). The IRs of DENV-1 and DENV-4 were significantly higher than those of DENV-2 and DENV-3 in all colonies (Table 4, Additional file 2). The lowest IR was observed for DENV-2 in the Ae. aegypti HCM and Ae. albopictus BSD colonies, and for DENV-3 in the Ae. albopictus IKT colony (Table 4, Additional file 2). The Ae. aegypti HCM colony had IRs > 60% for all serotypes (Table 4, Additional file 2). The Ae. albopictus colonies, however, tended to have large differences in IR between serotypes in both colonies, with the greatest difference in observed between serotypes: an approximately 5- to 6-fold difference in IR between DENV-4 and DENV-3 in the IKT colony and between DENV-1 and DENV-2 in the BSD colony (Table 4, Additional file 2).

Furthermore, comparison of viral RNA copy number between different serotypes in the same colony showed that in the thorax and abdomen, the RNA copy number of DENV-4 was significantly higher than that of the other serotypes in the Ae. aegypti HCM colony (Additional file 3). Regarding DENV RNA copy number in the thorax and abdomen of the Ae. albopictus colonies, DENV-4 was significantly higher than DENV-1 in the IKT colony and DENV-4 was significantly higher than DENV-3 in the BSD colony (Additional file 3). No significant copy number differences were observed between the other serotypes in both Ae. albopictus colonies.

Status of dengue virus dissemination in mosquito species and colonies

In contrast to the IR, no significant differences in dissemination status for DENV-1 and DENV-4 were observed between the Ae. aegypti HCM and Ae. albopictus BSD colonies; however, both had a significantly higher DR than that of the Ae. albopictus IKT colony (Fig. 1B, Table 4). In contrast, for DENV-2 and DENV-3, the Ae. aegypti HCM colony had a significantly higher DR than that of both Ae. albopictus colonies, similar to the IR results, and no significant differences were observed between the Ae. albopictus colonies (Fig. 1B, Table 4). The greatest difference in DR (14-fold) was observed for DENV-3 between Ae. aegypti HCM and Ae. albopictus IKT colonies (Table 4).

For DENV-1 and DENV-4, DENV RNA was detected in the head, wings, and legs of all individuals in the BSD colony in which viral RNA was detected in the thorax and abdomen (Additional file 4). Similarly, in the Ae. aegypti HCM colony, viral RNA was detected in the head, wings, and legs of 100% of the individuals that were positive for DENV-4 RNA in the thorax and abdomen (Additional file 4).

A comparison of DENV RNA copy numbers in the head, wings, and legs between species and colonies revealed that only the DENV-1 copy number was significantly higher in the Ae. aegypti HCM colony than in both Ae. albopictus colonies (Fig. 2B). The RNA copy number of DENV-4 was significantly higher in the Ae. aegypti HCM colony than in the Ae. albopictus IKT colony, but otherwise there were no significant differences observed between the species and/or colonies (Fig. 2B).

In addition, DR by serotype was also compared in each colony (Additional file 5). The Ae. aegypti HCM colony showed a DR higher than 50% for all serotypes, although there were significant differences among them (Table 4, Additional file 5). Even among the serotypes with the greatest differences in DR, these differences were less than twofold. In the Ae. albopictus colonies, however, the difference in DR between serotypes was greater than that observed for IR, with an approximate eightfold difference in DR between DENV-3 and DENV-4 in the IKT colony and an approximate 11-fold difference in DR between DENV-1 and DENV-2 in the BSD colony (Table 4, Additional file 5).

Furthermore, there were almost no significant differences in viral RNA copy numbers in the head, wings, and legs between serotypes, and those of DENV-1 and DENV-4 were significantly higher than that of DENV-3 only in the Ae. aegypti HCM colony (Additional file 6).

Discussion

In this study, all DENV serotypes could infect Japanese Ae. albopictus mosquitoes, and their susceptibility to the virus was compared with that of Ae. aegypti, the main vector of DENV. The titers of DENV used for infection experiments were 0.72–7.17 × 106 FFU/mL. This is within the range of serum viral titers of imported cases observed in Japan [1.0 × 102–2.9 × 107 plaque forming units (PFU)/mL] [30] and close to the mean viral titer of imported cases (1.3 × 107 PFU /mL) reported in another study [31]. Therefore, the DENV titers used in this infection experiment were considered adequate.

Results of the infection experiments showed that Japanese Ae. albopictus was infectious with all DENV serotypes, and viruses were also detected in the head, wings, and legs, indicating that all serotypes exhibited systemic infection. However, the IR of the Japanese Ae. albopictus, i.e., viral infection of the thorax and abdomen, including the midgut, was significantly lower than that of Ae. aegypti for all DENV serotypes. This suggests that viral infection is inhibited by the midgut infection barrier, which is the first barrier against viral infection [32]. More than half of Ae. albopictus individuals with confirmed DENV infections in the thorax and abdomen had DENV RNA detected in their head, wings, and legs, indicating a similar level of dissemination dynamic as that in Ae. aegypti. Furthermore, DENV-1 was also found to be more efficiently disseminated in a certain Ae. albopictus colony than in Ae. aegypti. In addition, there was almost no difference in the number of DENV RNA copies between Ae. aegypti and Ae. albopictus colonies. This suggests that Japanese Ae. albopictus might transmit the virus to the same extent as Ae. aegypti, depending on the DENV serotype. However, the extent to which these viruses are expelled with mosquito saliva was not investigated in this study; therefore, further research is needed to confirm the ability of Japanese Ae. albopictus to transmit the DENV serotypes.

This study showed that Japanese Ae. albopictus have large differences in IR and DR among the DENV serotypes. This is consistent with data observed in previous studies on Ae. albopictus that show differences in susceptibility to DENV serotypes [33, 34]. The results of the present study confirmed that DENV-1 and DENV-4 infected both Ae. albopictus colonies more efficiently than serotypes 2 and 3. However, the virus titers used in the infection experiments in this study differed between serotypes, and it is possible that differences in the initial amount of virus sucked by the mosquitoes may have affected their subsequent susceptibility. Moreover, in this study, only a certain of the many genotypes of each DENV serotype were used in the experiments. Previous studies have reported that mosquito susceptibility to different viral genotypes within the same serotype also varies [35,36,37]. Therefore, we expect that future studies using genotypes other than those used in this study could reveal more detailed differences in the susceptibility of Japanese Ae. albopictus to different DENV serotypes.

To date, several outbreaks of dengue fever have been reported in temperate zones in Japan and Europe, where Ae. albopictus was the only mosquito vector (Table 1). Despite the identification of imported cases with different DENV serotypes in these regions [38, 39], the majority of autochthonous epidemics have been caused by DENV-1 (Table 1). Additionally, DENV-1 is the only or major epidemic serotype caused in dengue epidemics even in tropical and subtropical regions where Ae. albopictus was the sole vector mosquito [8,9,10]. Thus, many outbreaks of Ae. albopictus as the main vector were caused by DENV-1. Since DENV-1 used in this study is a Japanese epidemic strain [28], the possibility that it was already adapted to Ae. albopictus cannot be ruled out, but it showed high infectivity and propagation in Japanese Ae. albopictus among the serotypes tested. This suggests that Ae. albopictus is highly compatible with DENV-1. Therefore, DENV-1 is more likely to spread during an epidemic in which Ae. albopictus is the primary vector. In addition, results of this study indicated that Ae. albopictus is as highly susceptible to DENV-4 as it is to DENV-1. To date, DENV-4 has not been prevalent in outbreaks in which Ae. albopictus was the primary vector. However, based on results of the present study, there may be a risk of future outbreaks of this serotype in areas where Ae. albopictus is the dominant vector.

Conclusions

In the present study, we investigated the susceptibility of Japanese Ae. albopictus to DENV and compared its IR, DR, and DENV propagation efficiency with those of Ae. aegypti, the main vector of DENV. The analyses revealed for the first time that Japanese Ae. albopictus was susceptible to all DENV serotypes. Compared with that of Ae. aegypti, a higher percentage of Japanese Ae. albopictus had an inhibitory effect on DENV infection via the midgut infection barrier. However, once the virus overcomes this barrier, it propagates and disseminates to the hemocoel and other tissues in Ae. albopictus as efficiently as that in Ae. aegypti. Based on previous dengue outbreak trends and the results of the infection experiment in this study, Ae. albopictus is predicted to be highly compatible with DENV-1, suggesting that this serotype poses a high risk for future epidemics in Japan.

Availability of data and materials

The datasets supporting the conclusions of this article are included within the article and its additional files.

Abbreviations

D:

Dark

DENV:

Dengue virus

DENV-1:

Dengue virus serotype 1

DENV-2:

Dengue virus serotype 2

DENV-3:

Dengue virus serotype 3

DENV-4:

Dengue virus serotype 4

DR:

Dissemination rate

FFU:

Focus forming units

IR:

Infection rate

L:

Light

PFU:

Plaque forming units

RT-PCR:

Reverse transcription polymerase chain reaction

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Acknowledgements

None.

Funding

This work was supported by grants-in-aid from Japan Agency for Medical Research and development (AMED) Grant Numbers JP18fk0108067, JP20wm0225007, JP21fk0108613, JP23fk0108656, and JP23wm0225030, and JSPS KAKENHI Grant Number JP63K05257.

Author information

Author notes

  1. Meng Ling Moi

    Present address: Department of Developmental Medical Sciences, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan

  2. Tomohiko Takasaki

    Present address: BML, Inc., Tokyo, Japan

  3. Daisuke Kobayashi and Izumi Kai have contributed equally to this work.

Authors and Affiliations

  1. Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan

    Daisuke Kobayashi, Izumi Kai, Astri Nur Faizah, Toshinori Sasaki & Haruhiko Isawa

  2. Management Department of Biosafety, Laboratory Animal, and Pathogen Bank, National Institute of Infectious Diseases, Tokyo, Japan

    Daisuke Kobayashi

  3. Graduate School of Agriculture, Meiji University, Kanagawa, Japan

    Izumi Kai

  4. Department of Virology I, National Institute of Infectious Diseases, Tokyo, Japan

    Meng Ling Moi, Shigeru Tajima & Tomohiko Takasaki

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  1. Daisuke Kobayashi
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Contributions

DK designed the study; MML, ST, TT, and TS prepared and provided experimental materials; DK, IK and FAN conducted the experiment and data analysis; HI supervised the study; DK wrote the manuscript draft. All authors have reviewed and approved the manuscript.

Corresponding author

Correspondence to Daisuke Kobayashi.

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Ethics approval and consent to participate

Not applicable. The dengue virus strains used in this study were those isolated in previous studies, and this study itself does not involve the use of human data or tissues.

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Not applicable.

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The authors declare that they have no competing interests.

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Supplementary Information

Additional file 1.

List of primers and probes used in this study.

Additional file 2.

Comparison of the infection rates of dengue virus serotypes in each mosquito species and colony.

Additional file 3.

Comparison of dengue virus serotype propagation in Aedes aegypti and Japanese Ae. albopictus colonies.

Additional file 4.

Dissemination rate of Aedes aegypti and Japanese Ae. albopictus colonies.

Additional file 5.

Comparison of the dissemination rates of dengue virus serotypes in each mosquito species and colony.

Additional file 6.

Comparison of dengue virus serotype propagation in Aedes aegypti and Japanese Ae. albopictus colonies.

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Kobayashi, D., Kai, I., Faizah, A.N. et al. Comparative analysis of the susceptibility of Aedes aegypti and Japanese Aedes albopictus to all dengue virus serotypes. Trop Med Health 51, 61 (2023). https://doi.org/10.1186/s41182-023-00553-5

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Keywords

Tropical Medicine and Health

ISSN: 1349-4147

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