bims-mosdis Biomed News
on Mosquito distribution and disease
Issue of 2021–10–17
fiveteen papers selected by
Richard Halfpenny, Staffordshire University



  1. Parasit Vectors. 2021 Oct 11. 14(1): 527
      The expansion of mosquito-borne diseases such as dengue, yellow fever, and chikungunya in the past 15 years has ignited the need for active surveillance of common and neglected mosquito-borne infectious diseases. The surveillance should be designed to detect diseases and to provide relevant field-based data for developing and implementing effective control measures to prevent outbreaks before significant public health consequences can occur. Mosquitoes are important vectors of human and animal pathogens, and knowledge on their biodiversity and distribution in the Afrotropical region is needed for the development of evidence-based vector control strategies. Following a comprehensive literature search, an inventory of the diversity and distribution of mosquitoes as well as the different mosquito-borne diseases found in Cameroon was made. A total of 290 publications/reports and the mosquito catalogue website were consulted for the review. To date, about 307 species, four subspecies and one putative new species of Culicidae, comprising 60 species and one putative new species of Anopheles, 67 species and two subspecies of Culex, 77 species and one subspecies of Aedes, 31 species and one subspecies of Eretmapodites, two Mansonia, eight Coquillettidia, and 62 species with unknown medical and veterinary importance (Toxorhynchites, Uranotaenia, Mimomyia, Malaya, Hodgesia, Ficalbia, Orthopodomyia, Aedeomyia, and Culiseta and Lutzia) have been collected in Cameroon. Multiple mosquito species implicated in the transmission of pathogens within Anopheles, Culex, Aedes, Eretmapodites, Mansonia, and Coquillettidia have been reported in Cameroon. Furthermore, the presence of 26 human and zoonotic arboviral diseases, one helminthic disease, and two protozoal diseases has been reported. Information on the bionomics, taxonomy, and distribution of mosquito species will be useful for the development of integrated vector management programmes for the surveillance and elimination of mosquito-borne diseases in Cameroon.
    Keywords:  Arboviruses; Biodiversity; Cameroon; Distribution; Lymphatic filariasis; Malaria; Mosquito; Mosquito-borne diseases
    DOI:  https://doi.org/10.1186/s13071-021-04950-9
  2. Malar J. 2021 Oct 10. 20(1): 397
       BACKGROUND: In rural Burkina Faso, the primary malaria vector Anopheles gambiae sensu lato (s.l.) primarily feeds indoors at night. Identification of factors which influence mosquito house entry could lead to development of novel malaria vector control interventions. A study was therefore carried out to identify risk factors associated with house entry of An. gambiae s.l. in south-west Burkina Faso, an area of high insecticide resistance.
    METHODS: Mosquitoes were sampled monthly during the malaria transmission season using CDC light traps in 252 houses from 10 villages, each house sleeping at least one child aged five to 15 years old. Potential risk factors for house entry of An. gambiae s.l. were measured, including socio-economic status, caregiver's education and occupation, number of people sleeping in the same part of the house as the child, use of anti-mosquito measures, house construction and fittings, proximity of anopheline aquatic habitats and presence of animals near the house. Mosquito counts were compared using a generalized linear mixed-effect model with negative binomial and log link function, adjusting for repeated collections.
    RESULTS: 20,929 mosquitoes were caught, of which 16,270 (77.7%) were An. gambiae s.l. Of the 6691 An. gambiae s.l. identified to species, 4101 (61.3%) were An. gambiae sensu stricto and 2590 (38.7%) Anopheles coluzzii. Having a metal-roof on the child's sleeping space (IRR = 0.55, 95% CI 0.32-0.95, p = 0.03) was associated with fewer malaria vectors inside the home.
    CONCLUSION: This study demonstrated that the rate of An. gambiae s.l. was 45% lower in sleeping spaces with a metal roof, compared to those with thatch roofs. Improvements in house construction, including installation of metal roofs, should be considered in endemic areas of Africa to reduce the burden of malaria.
    DOI:  https://doi.org/10.1186/s12936-021-03926-5
  3. PLoS One. 2021 ;16(10): e0255321
       BACKGROUND: An. funestus is a major Afrotropical vector of human malaria. This study sought to investigate the larval ecology, sporozoite infection rates and blood meal sources of An. funestus in western Kenya.
    METHODS: Larval surveys were carried out in Bungoma (Highland) and Kombewa (lowland) of western Kenya. Aquatic habitats were identified, characterized, georeferenced and carefully examined for mosquito larvae and predators. Indoor resting mosquitoes were sampled using pyrethrum spray catches. Adults and larvae were morphologically and molecularly identified to species. Sporozoite infections and blood meal sources were detected using real-time PCR and ELISA respectively.
    RESULTS: Of the 151 aquatic habitats assessed, 62/80 (78%) in Bungoma and 58/71(82%) in Kombewa were positive for mosquito larvae. Of the 3,193 larvae sampled, An. funestus larvae constitute 38% (1224/3193). Bungoma recorded a higher number of An. funestus larvae (85%, 95%, CI, 8.722-17.15) than Kombewa (15%, 95%, CI, 1.33-3.91). Molecular identification of larvae showed that 89% (n = 80) were An. funestus. Approximately 59%, 35% and 5% of An. funestus larvae co-existed with An. gambiae s.l, Culex spp and An. coustani in the same habitats respectively. Of 1,221 An. funestus s.l adults sampled, molecular identifications revealed that An. funestus constituted 87% (n = 201) and 88% (n = 179) in Bungoma and Kombewa, respectively. The Plasmodium falciparum sporozoite rate of An. funestus in Bungoma and Kombewa was 2% (3/174) and 1% (2/157), respectively, and the human blood index of An. funestus was 84% (48/57) and 89% (39/44) and for Bungoma and Kombewa, respectively.
    CONCLUSION: Man-made ponds had the highest abundance of An. funestus larvae. Multiple regression and principal component analyses identified the distance to the nearest house as the key environmental factor associated with the abundance of An. funestus larvae in aquatic habitats. This study serves as a guide for the control of An. funestus and other mosquito species to complement existing vector control strategies.
    DOI:  https://doi.org/10.1371/journal.pone.0255321
  4. Vector Borne Zoonotic Dis. 2021 Oct 14.
      Mosquitoes transmit several pathogens in tropical regions, especially in forest areas. The diseases caused by these pathogens include malaria and several arboviruses such as yellow fever. Brazil has the largest endemic area in the world for yellow fever. Many factors can affect the sylvatic cycle of the disease, shifting it into human-inhabited areas. This study aims to examine the oviposition behavior of mosquito species that are effective or potential vectors of the yellow fever virus and which colonize bamboo traps and ovitraps installed at different heights. The positions of the traps in the strata were changed every 15 days. The collection of immature stages (eggs, larvae, and pupae) was performed every 2 weeks for 12 months from August 2018 to July 2019 in the city of Nova Iguaçu, state of Rio de Janeiro, Brazil, in an area near the Tinguá Biological Reserve (REBIO) in the districts of Adrianópolis and Rio D'ouro. Statistical tests were used to compare oviposition at each stratum, and correlation tests showed the relationship between the presence of eggs and immature mosquitoes (larvae and pupae) and temperature, precipitation, and trap type. The diversity was calculated for each trap type and height, as well as the dry and rainy seasons. During the sampling period, 3929 eggs and 4953 larvae and pupae were collected. The traps installed in the high strata remained empty when traps on the ground were installed at the same time, although not when they were installed on their own. The results obtained with this new proposed methodology suggest that diversity is greatest in the rainy season and in bamboo traps for either stratum. Furthermore, this study suggests that mosquitoes begin searching for breeding sites at ground level. Higher levels may be occupied due to the absence or impermanence of other breeding sites.
    Keywords:  bamboo trap; breeding; mosquito; ovitrap; strata
    DOI:  https://doi.org/10.1089/vbz.2021.0033
  5. Am J Trop Med Hyg. 2021 Oct 11. pii: tpmd200808. [Epub ahead of print]
      The mosquito Aedes aegypti transmits arboviral diseases at extraordinary rates. Dengue alone afflicts 50 to 100 million people each year, with more than 3 billion at risk globally. This indicates that current approaches to prevention and control are inadequate, and that a paradigm shift from one that largely promotes vertical chemical-based control and vaccine development to one that also concentrates on eliminating the mosquito through actions by the communities it plagues is necessary. We have developed a new social and software platform, DengueChat (denguechat.org), to advance community interventions in arbovirus vector control. It is an interactive platform combining open-source digital communication technologies with face-to-face assemblies. It promotes resident participation in evidence collection, reporting, and analysis, and it incorporates pedagogic information, key messaging, and game concepts to motivate communities to implement vector reduction strategies. Using DengueChat, we conducted a 19-month pilot study in five neighborhoods of Managua, Nicaragua. The results strongly suggest that using the software produced value-added features that enhance community engagement. We measured the entomological and behavioral impacts at different time points and relative risk reduction of entomological indices at the end of the study. The entomological results showed significant risk reductions in disease transmission: Ae. aegypti larvae and pupae indices were reduced by approximately 44% in neighborhoods using DengueChat during one epidemic year, whereas control neighborhoods experienced an increase of more than 500%. A cluster permutation test determined that the probability of household positivity was significantly reduced in neighborhoods that participated in DengueChat compared with the reference neighborhoods (P = 0.0265). Therefore, DengueChat is a promising resource for vector control.
    DOI:  https://doi.org/10.4269/ajtmh.20-0808
  6. Parasit Vectors. 2021 Oct 14. 14(1): 534
       BACKGROUND: Aedes koreicus is a mosquito species characterized by marked anthropophilic behavior, and a potential vector of nematodes and viruses. It is native to East Asia, but its presence has recently been reported in many regions of Europe. In Italy, these mosquitoes had been detected in the northeast since 2011 and are now spreading towards the southwest of the country.
    METHODS: In 2020, during a surveillance program for invasive mosquito species in the district of Bergamo (Lombardy Region, Italy), about 6000 mosquito larvae were collected. Emerged adults were assigned to mosquito species according to morphological analyses, followed by amplification and sequencing of genetic markers (COI, ND4, ITS2 and D2).
    RESULTS: According to the morphological and genetic data, about 50 individuals belonged to the species Ae. koreicus.
    CONCLUSION: We report the presence of Ae. koreicus in the district of Bergamo, which confirms the spread of this species in the north of Italy and raises concerns about its possible role as a vector of diseases in the Alpine area.
    Keywords:  Aedes koreicus; Alien species; Invasive mosquitoes; Morphological and molecular identification
    DOI:  https://doi.org/10.1186/s13071-021-05031-7
  7. Sci Rep. 2021 Oct 12. 11(1): 20241
      Culex pipiens pallens is an important vector of lymphatic filariasis and epidemic encephalitis. Mosquito control is the main strategy used for the prevention of mosquito-borne diseases. Bacillus thuringiensis israelensis (Bti) is an entomopathogenic bacterium widely used in mosquito control. In this study, we profiled the microbiota and transcriptional response of the larvae of Cx. pipiens pallens exposed to different concentrations of Bti. The results demonstrated that Bti induced a significant effect on both the microbiota and gene expression of Cx. pipiens pallens. Compared to the control group, the predominant bacteria changed from Actinobacteria to Firmicutes, and with increase in the concentration of Bti, the abundance of Actinobacteria was gradually reduced. Similar changes were also detected at the genus level, where Bacillus replaced Microbacterium, becoming the predominant genus in Bti-exposed groups. Furthermore, alpha diversity analysis indicated that Bti exposure changed the diversity of the microbota, possibly because the dysbiosis caused by the Bti infection inhibits some bacteria and provides opportunities to other opportunistic taxa. Pathway analysis revealed significant enhancement for processes associated with sphingolipid metabolism, glutathione metabolism and glycerophospholipid metabolism between all Bti-exposed groups and control group. Additionally, genes associated with the Toll and Imd signaling pathway were found to be notably upregulated. Bti infection significantly changed the bacterial community of larvae of Cx. pipiens pallens.
    DOI:  https://doi.org/10.1038/s41598-021-99733-8
  8. J Insect Physiol. 2021 Oct 07. pii: S0022-1910(21)00129-3. [Epub ahead of print] 104319
      Resistance to currently utilized chemical insecticidal agents represents a significant threat to public health and food security worldwide. Better understanding the neurophysiological effects of available and candidate insecticidal molecules is valuable for characterizing the mechanisms of insecticide resistance, as well as the design and study of novel control chemistries. In this paper, we describe a method of recording nerve firing from the central nervous system of Aedes aegypti fourth instar larvae. In short, mosquito larvae were immobilized by placing small pins through the head and siphon of the larvae in a wax dish, ventral side down. A single, longitudinal, dorsal incision from the distal abdomen to the pronotum of the larva was made, the alimentary canal removed, and the ventral nerve cord severed between the second and third abdominal ganglia. A recording suction electrode was connected directly to axons within the severed end of the connective in a novel way to record nerve firing in the ventral nerve cord at high signal-to-noise ratio with conventional electrophysiological equipment. Using this novel method, we report the effects of four neuroactive compounds using this method: octopamine, pilocarpine, nicotine, and γ-aminobutyric acid (GABA). The utility of this recording technique for elucidating target site mechanisms involved in insecticide resistance is demonstrated with p,p'-dichlorodiphenyltrichlorethane (DDT) and its difluoro analog (DFDT).
    Keywords:  Aedes aegypti; DDT; DFDT; central nervous system; mosquito neurophysiology
    DOI:  https://doi.org/10.1016/j.jinsphys.2021.104319
  9. EBioMedicine. 2021 Oct 06. pii: S2352-3964(21)00389-3. [Epub ahead of print]72 103596
       BACKGROUND: Nicaragua experienced a large Zika epidemic in 2016, with up to 50% of the population in Managua infected. With the domesticated Aedes aegypti mosquito as its vector, it is widely assumed that Zika virus transmission occurs within the household and/or via human mobility. We investigated these assumptions by using viral genomes to trace Zika transmission spatially.
    METHODS: We analysed serum samples from 119 paediatric Zika cases participating in the long-standing Paediatric Dengue Cohort Study in Managua, which was expanded to include Zika in 2015. An optimal spanning directed tree was constructed by minimizing the differences in viral sequence diversity composition between patient nodes, where low-frequency variants were used to increase the resolution of the inferred Zika outbreak dynamics.
    FINDINGS: Out of the 18 houses where pairwise difference in sample collection dates among all the household members was within 30 days, we only found two where viruses from individuals within the same household were up to 10th-most closely linked to each other genetically. We also identified a substantial number of transmission events involving long geographical distances (n=30), as well as potential super-spreading events in the estimated transmission tree.
    INTERPRETATION: Our finding highlights that community transmission, often involving long geographical distances, played a much more important role in epidemic spread than within-household transmission.
    FUNDING: This study was supported by an NUS startup grant (OMS) and grants R01 AI099631 (AB), P01 AI106695 (EH), P01 AI106695-03S1 (FB), and U19 AI118610 (EH) from the US National Institutes of Health.
    Keywords:  Nicaragua; Zika virus; genomic inference; transmission network
    DOI:  https://doi.org/10.1016/j.ebiom.2021.103596
  10. Nat Commun. 2021 Oct 14. 12(1): 6018
      Mosquito bites transmit a number of pathogens via salivary droplets deposited during blood-feeding, resulting in potentially fatal diseases. Little is known about the genomic content of these nanodroplets, including the transmission dynamics of live pathogens. Here we introduce Vectorchip, a low-cost, scalable microfluidic platform enabling high-throughput molecular interrogation of individual mosquito bites. We introduce an ultra-thin PDMS membrane which acts as a biting interface to arrays of micro-wells. Freely-behaving mosquitoes deposit saliva droplets by biting into these micro-wells. By modulating membrane thickness, we observe species-dependent differences in mosquito biting capacity, utilizable for selective sample collection. We demonstrate RT-PCR and focus-forming assays on-chip to detect mosquito DNA, Zika virus RNA, as well as quantify infectious Mayaro virus particles transmitted from single mosquito bites. The Vectorchip presents a promising approach for single-bite-resolution laboratory and field characterization of vector-pathogen communities, and could serve as a powerful early warning sentinel for mosquito-borne diseases.
    DOI:  https://doi.org/10.1038/s41467-021-26300-0
  11. Virol J. 2021 Oct 12. 18(1): 204
       BACKGROUND: Arbovirus surveillance and recurrence of outbreaks in Kenya continues to reveal the re-emergence of viruses of public health importance. This calls for sustained efforts in early detection and characterization of these agents to avert future potential outbreaks.
    METHODS: A larval survey was carried out in three different sites in Kwale County, Vanga, Jego and Lunga Lunga. All containers in every accessible household and compound were sampled for immature mosquitoes. In addition, adult mosquitoes were also sampled using CO2-baited CDC light traps and BG-Sentinel traps in the three sites and also in Tsuini. The mosquitoes were knocked down using trimethylamine and stored in a liquid nitrogen shipper for transportation to the laboratory where they were identified to species, pooled and homogenized ready for testing.
    RESULTS: A total of 366 houses and 1730 containers were inspected. The House Index (HI), Container Index (CI) and Breateau Index (BI) for Vanga Island were (3%: 0.66: 3.66) respectively. In Jego, a rural site, the HI, CI and BI were (2.4%: 0.48: 2.4) respectively. In Lunga Lunga, a site in an urban area, the HI, CI and BI were (22.03%: 3.97: 29.7) respectively. The indices suggest that this region is at risk of arbovirus transmission given they were above the WHO threshold (CI > 1, HI > 1% and BI > 5). The most productive containers were the concrete tanks (44.4%), plastic tank (22.2%), claypot (13.3%), plastic drums (8.9%), plastic basins (4%), jerricans (1.2%) and buckets (0.3%). Over 20,200 adult mosquitoes were collected using CDC light traps, and over 9,200 using BG- sentinel traps. These mosquitoes were screened for viruses by inoculating in Vero cells. Eleven Orthobunyavirus isolates were obtained from pools of Ae. pembaensis (4), Ae. tricholabis (1), Cx. quinquefasciatus (3), Culex spp. (1) and Cx. zombaensis (2). Five of the Orthobunyaviruses were sequenced and four of these were determined to be Bunyamwera viruses while one isolate was found to be Nyando virus. One isolate remained unidentified.
    CONCLUSIONS: These results indicate circulation of Orthobunyaviruses known to cause diverse grades of febrile illness with rash in humans in this region and highlights the need for continued monitoring and surveillance to avert outbreaks.
    Keywords:  Bunyamwera virus; Mosquitoes; Nyando virus; Orthobunyaviruses
    DOI:  https://doi.org/10.1186/s12985-021-01670-5
  12. Malar J. 2021 Oct 09. 20(1): 395
       BACKGROUND: Innovative tools are needed to complement the existing approach for malaria elimination. Gene drive mosquitoes are one potential new technology in the control of malaria vectors. Target Malaria is one of the research projects developing this technology, and in July 2019, the project proceeded to an important step for this evaluation pathway: the small-scale release of non-gene drive sterile male mosquitoes in a village in Burkina Faso. In addition to the entomological and laboratory work to prepare for this important milestone, significant community and stakeholder engagement work was done. The existing guidelines on gene drive mosquito provide an overall framework for such engagement work. However, they do not provide a road map on how to proceed or what benchmarks should be used to assess this work.
    METHODS: This study provides a review of engagement activities relevant to field trials on non-gene drive genetically-modified mosquitoes as well as an assessment framework-using both qualitative and quantitative studies as well as an audit procedure. The latter was implemented to evaluate whether the release activities could proceed with the appropriate level of agreement from the community.
    RESULTS: This paper shows the importance of this first phase of work to innovate and learn about engagement processes for responsible research in the field of genetic approaches for malaria vector control. The function of these assessments is crucial for the learning agenda. The assessments demonstrated ways to increase understanding and ensure effective progress with field studies and, therefore, the pathway for responsible research.
    CONCLUSION: Gene drive technology is increasingly considered as a promising approach to control vector borne diseases, in particular malaria. Stakeholders' involvement in this research process is one of the recurring requirements in international guidance documents. With this paper Target Malaria offers an opportunity to explore the practical achievements and challenges of stakeholder engagement during early phases of a technology evaluation, and in particular how it implemented an assessment framework to learn from its experience.
    Keywords:  Audit; Evaluation; Gene drive; Genetically modified mosquitoes release; Malaria; Responsible research; Stakeholder engagement
    DOI:  https://doi.org/10.1186/s12936-021-03929-2
  13. Lancet Planet Health. 2021 Oct;pii: S2542-5196(21)00203-5. [Epub ahead of print]5(10): e731-e738
       BACKGROUND: Guyana reported a significant rise in malaria between 2008 and 2014. As there was no evidence of impairment of national malaria control strategies, public health authorities attributed the surge to a temporal increase in gold mining activity in forested regions. However, systematic analysis of this association is lacking because of the difficulties associated with collecting reliable data for both malaria and mining. We aimed to investigate the association between the international gold price and Plasmodium falciparum malaria transmission in Guyana between 2007 and 2019. We also aimed to evaluate the association between P falciparum cases and the El Niño-Southern Oscillation pattern, which has previously been suggested as a major driver of malaria.
    METHODS: We used national malaria surveillance data from Guyana to estimate the correlation over time between the international gold price and reported P falciparum infections in individuals who were likely to be involved in mining activities (ie, men and boys aged between 15 and 50 years who were living in mining regions) for each month between 2007 and 2019. We compared the estimates with those obtained from individuals who were unlikely to be directly involved in mining activities (ie, women, children aged 12 years and younger, and adults aged over 70 years) and estimates obtained from individuals living in non-mining regions. We also evaluated the correlation between P falciparum infections and the El Niño-Southern Oscillation pattern in the same subpopulations and time period. Lastly, we evaluated the performance of a statistical model formulated to estimate P falciparum infections in real time using the international gold price as the predictor variable.
    FINDINGS: The proportion of P falciparum malaria cases in temporary residents, which was used as a proxy for circulating individuals involved in gold mining, was highest during the years of peak gold price (ie, between 2008 and 2014). Cases of malaria in all demographic groups showed a strong positive correlation with the gold price, but only in regions with mining camps (0·88 [95% CI 0·84-0·89] for boys and men aged between 15 and 50 years and 0·80 [0·73-0·85] for the aggregated population of women, children aged 12 years and younger, and adults older than 70 years). The highest correlation occurred earlier in men and boys aged between 15 and 50 years, the demographic most likely to be miners, suggesting that transmission in mining camps is followed by infections in the community. On the basis of these findings, we were able to reliably forecast P falciparum malaria trends using only the gold price as the predictor variable. A 1% increase in gold price was associated with a 2·13% increase in P falciparum infections after 1 month in the mining populations, and with a 1·63% increase after 2 months in the non-mining populations. Lastly, La Niña climatic events showed an additional, smaller positive correlation with malaria transmission.
    INTERPRETATION: Our analysis provides evidence that the P falciparum malaria surge observed in Guyana between 2008 and 2014 was likely to have been driven mainly by an increase in gold mining, while climate factors might have contributed synergistically. We propose that the international gold price over time is a useful indicator of malaria trends. We conclude that the feasibility of malaria elimination in Guyana, and in other areas in the Amazon where malaria and gold mining overlap, should be evaluated against the challenges posed by rapidly rising gold prices.
    FUNDING: Ramón Areces Foundation, National Institutes of Health, and National Institute of General Medical Sciences.
    DOI:  https://doi.org/10.1016/S2542-5196(21)00203-5
  14. Lancet Planet Health. 2021 Oct;pii: S2542-5196(21)00141-8. [Epub ahead of print]5(10): e739-e745
      Vector-borne diseases are particularly sensitive to changes in weather and climate. Timely warnings from surveillance systems can help to detect and control outbreaks of infectious disease, facilitate effective management of finite resources, and contribute to knowledge generation, response planning, and resource prioritisation in the long term, which can mitigate future outbreaks. Technological and digital innovations have enabled the incorporation of climatic data into surveillance systems, enhancing their capacity to predict trends in outbreak prevalence and location. Advance notice of the risk of an outbreak empowers decision makers and communities to scale up prevention and preparedness interventions and redirect resources for outbreak responses. In this Viewpoint, we outline important considerations in the advent of new technologies in disease surveillance, including the sustainability of innovation in the long term and the fundamental obligation to ensure that the communities that are affected by the disease are involved in the design of the technology and directly benefit from its application.
    DOI:  https://doi.org/10.1016/S2542-5196(21)00141-8
  15. Health Econ. 2021 Oct 13.
      While mosquito-borne diseases are currently most prevalent in mid-latitude countries, rising global temperatures could expand their range. This paper investigates whether one such disease, dengue, harms newborns. The empirical design exploits epidemiological patterns of the disease spreading. Dengue infection rates in the mother's municipality of residence which prevailed during the gestation period are instrumented with exogenous factors that determine dengue incidence in municipalities that have tight social connections to the maternal municipality. Using a large longitudinal dataset of Brazilian birth records, I find that a higher dengue rate during the third trimester of gestation has a detrimental effect on birth weight. In utero exposure to dengue also increases the probability of cesarean delivery and can lead to more serious consequences such as increased fetal and maternal mortality rates.
    Keywords:  birth; dengue; mortality; virus; weather; weight
    DOI:  https://doi.org/10.1002/hec.4436