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Acharya BK, Khanal L, Dhimal M. Increased thermal suitability elevates the risk of dengue transmission across the mid hills of Nepal. PLoS One 2025; 20:e0322031. [PMID: 40273130 PMCID: PMC12021130 DOI: 10.1371/journal.pone.0322031] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/11/2024] [Accepted: 03/14/2025] [Indexed: 04/26/2025] Open
Abstract
The burden of climate-sensitive, mosquito-borne diseases, including dengue, has significantly increased in recent years. Understanding the temporal and spatial variations of these diseases is essential for effectively controlling potential outbreaks. In this study, we utilized Moderate Resolution Imaging Spectroradiometer (MODIS) satellite land surface temperature (LST) data (MOD11A2) and a temperature-dependent mechanistic model (R0) to predict the monthly suitability for dengue transmission in Nepal from 2001 to 2020 for both mosquito vectors, Aedes aegypti and Ae. albopictus. We divided the study period into two episodes: 2001-2010, which we characterized as the period of dengue emergence, and 2011-2020, identified as the period of rapid expansion. We compared the thermal suitability across these two time periods. The results indicated that approximately half of Nepal is thermally suitable for dengue transmission for at least one month, with the maximum transmission risk lasting up to nine months each year, a trend that has more or less remained stable over the past 20 years. However, strong temporal dynamics were observed in the hilly regions and around major urban centers such as Kathmandu and Pokhara, where the length of thermal suitability extended up to six months for both vector species. Consequently, the population exposed to thermal suitability increased significantly on a monthly basis. Compared to the emergence period, the proportion of the population exposed to a suitable thermal environment for six months or longer each year increased by 18% for Ae. aegypti and 20% for Ae. albopictus. These findings provide evidence-based insights that could assist health authorities in the control and management of dengue in Nepal.
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Affiliation(s)
- Bipin Kumar Acharya
- Planetary Health Research Center, Kathmandu, Nepal
- Nepal Open University, Lalitpur, Nepal
- Nepal Geographical Society, Kathmandu, Nepal
| | - Laxman Khanal
- Central Department of Zoology, Institute of Science and Technology, Tribhuvan University, Kathmandu, Nepal
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2
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Ware-Gilmore F, Jones MJ, Mejia AJ, Dennington NL, Audsley MD, Hall MD, Sgrò CM, Buckley T, Anand GS, Jose J, McGraw EA. Evolution and adaptation of dengue virus in response to high-temperature passaging in mosquito cells. Virus Evol 2025; 11:veaf016. [PMID: 40330315 PMCID: PMC12054504 DOI: 10.1093/ve/veaf016] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/02/2024] [Revised: 02/14/2025] [Accepted: 04/23/2025] [Indexed: 05/08/2025] Open
Abstract
The incidence of arboviral diseases like dengue, chikungunya, and yellow fever continues to rise in association with the expanding geographic ranges of their vectors, Aedes aegypti and Aedes albopictus. The distribution of these vectors is believed to be driven in part by climate change and increasing urbanization. Arboviruses navigate a wide range of temperatures as they transition from ectothermic vectors (from 15°C to 35°C) to humans (37°C) and back again, but the role that temperature plays in driving the evolution of arboviruses remains largely unknown. Here, we passaged replicate dengue serotype-2 virus populations 10 times at either 26°C (Low) or 37°C (High) in C6/36 Aedes albopictus cells to explore the differences in adaptation to these thermal environments. We then deep-sequenced the resulting passaged dengue virus populations and tested their replicative fitness in an all-cross temperature regime. We also assessed the ability of the passaged viruses to replicate in the insect vector. While viruses from both thermal regimes accumulated substitutions, only those reared in the 37°C treatments exhibited nonsynonymous changes, including several in the E, or envelope protein, and multiple non-structural genes. Passaging at the higher temperature also led to reduced replicative ability at 26°C in both cells and mosquitoes. One of the mutations in the E gene involved the loss of a glycosylation site previously shown to reduce infectivity in the vector. These findings suggest that viruses selected for growth at higher ambient temperatures may experience tradeoffs between thermostability and replication in the vector. Such associations might also have implications for the suitability of virus transmission under a changing climate.
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Affiliation(s)
- Fhallon Ware-Gilmore
- Department of Entomology, The Pennsylvania State University, University Park, PA 16802, USA
- The Center for Infectious Disease Dynamics, The Pennsylvania State University, University Park, PA 16802, USA
| | - Matthew J Jones
- Department of Entomology, The Pennsylvania State University, University Park, PA 16802, USA
- Department of Biology, The Pennsylvania State University, University Park, PA 16802, USA
| | - Austin J Mejia
- Department of Entomology, The Pennsylvania State University, University Park, PA 16802, USA
- The Center for Infectious Disease Dynamics, The Pennsylvania State University, University Park, PA 16802, USA
| | - Nina L Dennington
- Department of Entomology, The Pennsylvania State University, University Park, PA 16802, USA
| | - Michelle D Audsley
- School of Biological Sciences, Monash University, Melbourne, VIC 3800, Australia
| | - Matthew D Hall
- School of Biological Sciences, Monash University, Melbourne, VIC 3800, Australia
| | - Carla M Sgrò
- School of Biological Sciences, Monash University, Melbourne, VIC 3800, Australia
| | - Theresa Buckley
- The Center for Infectious Disease Dynamics, The Pennsylvania State University, University Park, PA 16802, USA
- Department of Chemistry, The Pennsylvania State University, University Park, PA 16802, USA
| | - Ganesh S Anand
- The Center for Infectious Disease Dynamics, The Pennsylvania State University, University Park, PA 16802, USA
- Department of Chemistry, The Pennsylvania State University, University Park, PA 16802, USA
| | - Joyce Jose
- The Center for Infectious Disease Dynamics, The Pennsylvania State University, University Park, PA 16802, USA
- Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA 16802, USA
| | - Elizabeth A McGraw
- Department of Entomology, The Pennsylvania State University, University Park, PA 16802, USA
- Department of Biology, The Pennsylvania State University, University Park, PA 16802, USA
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3
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de Freitas AC, Santos E, Baldon L, de Mendonça S, Rezende FO, Moreira R, Sousa V, Lima M, Silva E, Ferreira F, de Almeida JPP, Amadou S, Marçal B, Comini S, Rocha M, Todjro Y, Leite TJ, Santos V, de Faria IJDS, Giovanetti M, Alcantara LCJ, Moreira LA, Ferreira A. Infectivity and Dissemination of Dengue Virus-1 in Different Aedes aegypti Populations Throughout Brazil. Trop Med Infect Dis 2025; 10:112. [PMID: 40278785 PMCID: PMC12030886 DOI: 10.3390/tropicalmed10040112] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/04/2025] [Revised: 04/10/2025] [Accepted: 04/16/2025] [Indexed: 04/26/2025] Open
Abstract
Dengue virus, one of the most prevalent mosquito-borne flaviviruses affecting humans globally, is primarily transmitted by the Aedes aegypti mosquito, which thrives in densely populated urban environments. Dengue incidence has surged in recent decades, becoming a major public health concern in many regions, particularly in Brazil, which has experienced recurrent outbreaks and reported over 6.6 million probable cases in the year of 2024. While the link between the mosquito vector and dengue transmission is well understood, the effects of different DENV types and their interactions with the vector capacity of natural mosquito populations are crucial for understanding disease dynamics. Here we report findings from experiments designed to analyze and compare the infectivity and dissemination of the DENV-1 strain among five Ae. aegypti populations collected from different regions of Brazil. When exposed to DENV-infected AG129 mice for blood feeding, these populations exhibited variations in infection rates and dissemination efficiency. Eight days post-infection, all populations demonstrated high infection rates, underscoring the substantial capacity of Brazilian Ae. aegypti populations to support the locally circulating DENV-1 strain. Our results demonstrate variation in Ae. aegypti vector competence across Brazil, revealing distinct patterns of DENV transmission efficiency. These findings highlight the necessity for geographically tailored control strategies, particularly in high-risk urban areas where outbreak potential is greatest.
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Affiliation(s)
- Amanda Cupertino de Freitas
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Ellen Santos
- Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 6627-Pampulha, Belo Horizonte 31270-901, Brazil; (E.S.); (E.S.); (F.F.); (J.P.P.d.A.); (S.A.); (Y.T.); (T.J.L.); (I.J.d.S.d.F.)
| | - Lívia Baldon
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Silvana de Mendonça
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Fernanda Oliveira Rezende
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Rafaela Moreira
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
- Laboratório de Ecologia do Adoecimento & Florestas NUPEB/ICEB, Universidade Federal de Ouro Preto, Ouro Preto 35402-163, Brazil
| | - Viviane Sousa
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Mariana Lima
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Emanuele Silva
- Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 6627-Pampulha, Belo Horizonte 31270-901, Brazil; (E.S.); (E.S.); (F.F.); (J.P.P.d.A.); (S.A.); (Y.T.); (T.J.L.); (I.J.d.S.d.F.)
| | - Flávia Ferreira
- Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 6627-Pampulha, Belo Horizonte 31270-901, Brazil; (E.S.); (E.S.); (F.F.); (J.P.P.d.A.); (S.A.); (Y.T.); (T.J.L.); (I.J.d.S.d.F.)
| | - João Paulo Pereira de Almeida
- Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 6627-Pampulha, Belo Horizonte 31270-901, Brazil; (E.S.); (E.S.); (F.F.); (J.P.P.d.A.); (S.A.); (Y.T.); (T.J.L.); (I.J.d.S.d.F.)
| | - Siad Amadou
- Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 6627-Pampulha, Belo Horizonte 31270-901, Brazil; (E.S.); (E.S.); (F.F.); (J.P.P.d.A.); (S.A.); (Y.T.); (T.J.L.); (I.J.d.S.d.F.)
| | - Bruno Marçal
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Sara Comini
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Marcele Rocha
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Yaovi Todjro
- Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 6627-Pampulha, Belo Horizonte 31270-901, Brazil; (E.S.); (E.S.); (F.F.); (J.P.P.d.A.); (S.A.); (Y.T.); (T.J.L.); (I.J.d.S.d.F.)
| | - Thiago Jiran Leite
- Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 6627-Pampulha, Belo Horizonte 31270-901, Brazil; (E.S.); (E.S.); (F.F.); (J.P.P.d.A.); (S.A.); (Y.T.); (T.J.L.); (I.J.d.S.d.F.)
| | - Viviane Santos
- Plataforma de PCR em Tempo Real, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil;
| | - Isaque João da Silva de Faria
- Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 6627-Pampulha, Belo Horizonte 31270-901, Brazil; (E.S.); (E.S.); (F.F.); (J.P.P.d.A.); (S.A.); (Y.T.); (T.J.L.); (I.J.d.S.d.F.)
| | - Marta Giovanetti
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
- Department of Sciences and Technologies for Sustainable Development and One Health, University of Campus Bio-Medico, 00128 Rome, Italy
| | - Luiz Carlos Junior Alcantara
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Luciano A. Moreira
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
| | - Alvaro Ferreira
- Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou-Fiocruz, Belo Horizonte 30190-002, Brazil; (A.C.d.F.); (L.B.); (S.d.M.); (F.O.R.); (R.M.); (V.S.); (M.L.); (B.M.); (S.C.); (M.R.); (M.G.); (L.C.J.A.); (L.A.M.)
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4
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Shocket MS, Bernhardt JR, Miazgowicz KL, Orakzai A, Savage VM, Hall RJ, Ryan SJ, Murdock CC. Mean daily temperatures predict the thermal limits of malaria transmission better than hourly rate summation. Nat Commun 2025; 16:3441. [PMID: 40216754 PMCID: PMC11992237 DOI: 10.1038/s41467-025-58612-w] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/19/2024] [Accepted: 03/27/2025] [Indexed: 04/14/2025] Open
Abstract
Temperature shapes the geographic distribution, seasonality, and magnitude of mosquito-borne disease outbreaks. Models predicting transmission often use mosquito and pathogen thermal responses measured at constant temperatures. However, mosquitoes live in fluctuating temperatures. Rate summation--non-linear averaging of trait values measured at constant temperatures-is commonly used to infer performance in fluctuating environments, but its accuracy is rarely validated. We measured three traits that impact transmission-bite rate, survival, fecundity-in a malaria mosquito (Anopheles stephensi) across three diurnal temperature ranges (0, 9, and 12 °C). We compared transmission thermal suitability models with temperature-trait relationships observed under constant temperatures, fluctuating temperatures, and those predicted by rate summation. We mapped results across An. stephenesi's native Asian and invasive African ranges. We found: 1) daily temperature fluctuation trait values substantially differ from both constant temperature experiments and rate summation; 2) rate summation partially captured decreases in performance near thermal optima, yet incorrectly predicted increases near thermal limits; and 3) while thermal suitability across constant temperatures did not perfectly capture fluctuating environments, it was better than rate summation for estimating and mapping thermal limits. Our study provides insight into methods for predicting mosquito-borne disease risk and emphasizes the need to improve understanding of organismal performance under fluctuating conditions.
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Affiliation(s)
- Marta S Shocket
- Lancaster Environment Centre, Lancaster University, Lancaster, UK.
- Department of Geography and the Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA.
- Department of Ecology and Evolutionary Biology and Department of Computational Medicine, University of California Los Angeles, Los Angeles, CA, USA.
| | - Joey R Bernhardt
- Department of Integrative Biology, University of Guelph, Guelph, ON, Canada
| | - Kerri L Miazgowicz
- Department of Infectious Diseases, University of Georgia, Athens, GA, USA
| | - Alyzeh Orakzai
- Odum School of Ecology, University of Georgia, Athens, GA, USA
| | - Van M Savage
- Department of Ecology and Evolutionary Biology and Department of Computational Medicine, University of California Los Angeles, Los Angeles, CA, USA
- Santa Fe Institute, Santa Fe, NM, USA
| | - Richard J Hall
- Department of Infectious Diseases, University of Georgia, Athens, GA, USA
- Odum School of Ecology, University of Georgia, Athens, GA, USA
- Center for the Ecology of Infectious Diseases, University of Georgia, Athens, GA, USA
| | - Sadie J Ryan
- Department of Geography and the Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA
| | - Courtney C Murdock
- Odum School of Ecology, University of Georgia, Athens, GA, USA.
- Center for the Ecology of Infectious Diseases, University of Georgia, Athens, GA, USA.
- Cornell University, Ithaca, NY, USA.
- Department of Infectious Diseases, University of Georgia, Athens, GA, USA.
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5
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Montgomery MJ, Harwood JF, Yougang AP, Wilson-Bahun TA, Tedjou AN, Keumeni CR, Wondji CS, Kamgang B, Kilpatrick AM. The effects of urbanization, temperature, and rainfall on Aedes aegypti and Aedes albopictus mosquito abundance across a broad latitudinal gradient in Central Africa. Parasit Vectors 2025; 18:135. [PMID: 40189559 PMCID: PMC11972486 DOI: 10.1186/s13071-025-06764-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/26/2024] [Accepted: 03/13/2025] [Indexed: 04/10/2025] Open
Abstract
BACKGROUND Urbanization can influence disease vectors by altering larval habitat, microclimates, and host abundance. The global increase in urbanization, especially in Africa, is likely to alter vector abundance and pathogen transmission. We investigated the effect of urbanization and weather on the abundance of two mosquitoes, Aedes aegypti and Aedes albopictus, and infection with dengue, chikungunya, and Zika viruses at 63 sites in six cities spanning a 900-km latitudinal range in Cameroon, Central Africa. METHODS We used human landing catches and backpack-mounted aspirators to sample mosquitoes and collected larval habitat, host availability, and weather (temperature, precipitation, humidity) data for each site in each city. We analyzed land use and land cover information and satellite photos at varying radii around sites (100 m to 2 km) to quantify the extent of urbanization and the number of structures around each site. We used a continuous urbanization index (UI; range 0-100) that increased with impermeable surface and decreased with forest cover. RESULTS Urbanization increased larval habitat, human host availability, and Ae. aegypti mosquito abundance. Aedes aegypti abundance increased 1.7% (95% CI 0.69-2.7%) with each 1 unit increase in the urbanization index in all six cities (Douala, Kribi, Yaounde, Ngaoundere, Garoua, and Maroua) with a 5.4-fold increase from UI = 0 to UI = 100, and also increased with rainfall. In contrast, Ae. albopictus abundance increased with urbanization in one city, but showed no influence of urbanization in two other cites. Across three cities, Ae. albopictus abundance increased with rainfall, temperature, and humidity. Finally, we did not detect Zika, dengue, or chikungunya viruses in any specimens, and found weak evidence of interspecific competition in analyses of adult population growth rates. CONCLUSIONS These results show that urbanization consistently increases Ae. aegypti abundance across a broad range of habitats in Central Africa, while effects on Ae. albopictus were more variable and the abundance of both species were influenced by rainfall. Future urbanization of Africa will likely increase Ae. aegypti abundance, and climate change will likely alter abundance of both species through changes in precipitation and temperature.
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Affiliation(s)
- Matthew J Montgomery
- U.S. Naval Medical Research Unit EURAFCENT, PSC 824, Box 23, FPO AE 09623, Naval Air Station Sigonella, Italy.
- Ecology and Evolutionary Biology Department, University of California Santa Cruz, 130 McAllister Way, Santa Cruz, CA, 95060, USA.
| | - James F Harwood
- U.S. Naval Medical Research Unit EURAFCENT, PSC 824, Box 23, FPO AE 09623, Naval Air Station Sigonella, Italy
| | - Aurelie P Yougang
- Centre for Research in Infectious Diseases, P.O. Box 13591, Yaoundé, Cameroon
| | | | - Armel N Tedjou
- Centre for Research in Infectious Diseases, P.O. Box 13591, Yaoundé, Cameroon
| | | | - Charles S Wondji
- Centre for Research in Infectious Diseases, P.O. Box 13591, Yaoundé, Cameroon
| | - Basile Kamgang
- Centre for Research in Infectious Diseases, P.O. Box 13591, Yaoundé, Cameroon
| | - A Marm Kilpatrick
- Ecology and Evolutionary Biology Department, University of California Santa Cruz, 130 McAllister Way, Santa Cruz, CA, 95060, USA.
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Aslan IH, Pourtois JD, Frans VF, Forstchen M, Goodman MC, Chamberlin AJ, Mitchell KR, Mari L, Lo NC, Lwiza KM, Diakite NR, Ouattara M, N’Goran EK, Wood CL, Tuan R, Allan F, Caldeira RL, Monteiro AM, Rohr J, Mordecai EA, De Leo GA. Seasonal temperature fluctuation and snail adaptive behaviors yield insights into the dynamics and distribution of schistosomiasis in Africa. RESEARCH SQUARE 2025:rs.3.rs-6264426. [PMID: 40195990 PMCID: PMC11975034 DOI: 10.21203/rs.3.rs-6264426/v1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 04/09/2025]
Abstract
The complex relationship between temperature and schistosomiasis, an environmentally mediated neglected tropical disease affecting 250 million people globally, with hyperendemicity mostly in Africa, is poorly characterized. Here, we explored how seasonal temperature fluctuation affects the persistence, dynamics, and geographic distribution of schistosomiasis in Africa. We used a temperature-sensitive, mechanistic model of schistosomiasis dynamics that accounts for the adaptive behaviors of intermediate snail hosts and derived the disease's thermal response curve for different patterns of seasonal temperature fluctuations. Changing the amplitude of seasonal temperature fluctuations can influence both the thermal optimum and critical thermal thresholds which imply accurately drawing the thermal response curves requires accounting for seasonality in addition to mean annual temperature. Moreover, our simulations can reproduce the documented persistence of schistosomiasis at locations with strong seasonal temperature fluctuations and mean annual temperatures near or above the critical thermal maxima for snail hosts only when snail adaptive behavior (e.g., aestivation, movement into cooler depths or shade) is included in the model. These results suggest that future climate change impacting the amplitude and timing of these fluctuations will likely alter the future geographic distribution of schistosomiasis in African regions. Our work demonstrates that a comprehensive understanding of schistosomiasis and, potentially, other environmentally mediated diseases in Africa, necessitates the inclusion of seasonal temperature fluctuations and host behavioral adaptations in process-based mechanistic models.
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Affiliation(s)
- Ibrahim Halil Aslan
- Department of Biology, Stanford University, Stanford, CA, USA
- Hopkins Marine Station, Stanford University, Pacific Grove, CA, USA
| | - Julie D. Pourtois
- Department of Biology, University of Maryland, College Park, MD, USA
| | | | - Meghan Forstchen
- Department of Biology, University of Notre Dame, Notre Dame, IN, USA
| | - Maurice C. Goodman
- School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, USA
| | | | - Kaitlyn R. Mitchell
- Department of Biology, Stanford University, Stanford, CA, USA
- Hopkins Marine Station, Stanford University, Pacific Grove, CA, USA
| | - Lorenzo Mari
- Department of Electronics, Information and Bioengineering, Politecnico di Milano, Milano, Italy
| | - Nathan C. Lo
- Division of Infectious Diseases and Geographic Medicine, Department of Medicine, Stanford University, Stanford, CA, USA
| | - Kamazima M. Lwiza
- School of Marine and Atmospheric Sciences. Stony Brook University, New York, NY, USA
| | - Nana R. Diakite
- Université Félix Houphouët-Boigny, 22 BP 770, Abidjan 22, Côte d’Ivoire
| | - Mamadou Ouattara
- Université Félix Houphouët-Boigny, 22 BP 770, Abidjan 22, Côte d’Ivoire
| | | | - Chelsea L. Wood
- School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, USA
| | - Roseli Tuan
- Pasteur Institute, São Paulo Health Public Office, São Paulo, SP, Brazil
| | - Fiona Allan
- Department of Life Sciences, Natural History Museum, London, UK
| | | | | | - Jason Rohr
- Department of Biology, University of Notre Dame, Notre Dame, IN, USA
| | - Erin A. Mordecai
- Department of Biology, Stanford University, Stanford, CA, USA
- Woods Institute for the Environment, Stanford University, Stanford, CA, USA
| | - Giulio A. De Leo
- Hopkins Marine Station, Stanford University, Pacific Grove, CA, USA
- Woods Institute for the Environment, Stanford University, Stanford, CA, USA
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7
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Abbasi E. Climate Change and Vector-Borne Disease Transmission: The Role of Insect Behavioral and Physiological Adaptations. Integr Org Biol 2025; 7:obaf011. [PMID: 40330693 PMCID: PMC12053451 DOI: 10.1093/iob/obaf011] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/23/2025] [Revised: 03/16/2025] [Accepted: 03/18/2025] [Indexed: 05/08/2025] Open
Abstract
Climate change is profoundly reshaping the behavior, physiology, and distribution of insect vectors, with significant implications for vector-borne disease transmission. Rising temperatures, shifting precipitation patterns, and extreme weather events are driving behavioral adaptations such as altered host-seeking patterns, modified resting site preferences, and extended seasonal activity. Concurrently, vectors exhibit physiological plasticity, including enhanced thermal tolerance, desiccation resistance, and accelerated reproductive cycles, which contribute to increased survival and vector competence. This review synthesizes current research on climate-driven adaptations in major disease vectors, focusing on their epidemiological consequences and implications for public health interventions. A systematic literature review was conducted using major scientific databases to assess the impact of climate change on insect vector adaptation. Studies examining temperature-induced behavioral shifts, physiological modifications, and changes in vector competence were analyzed to identify emerging trends and knowledge gaps. Findings indicate that climate-driven vector adaptations are increasing the efficiency of disease transmission, enabling the geographic expansion of vector populations and prolonging transmission seasons. These changes challenge existing vector control strategies, necessitating innovative approaches such as genetic engineering, microbiome-based interventions, and climate-informed surveillance systems. Given the accelerating impact of climate change, there is an urgent need for adaptive, evidence-based control strategies to mitigate the growing threat of vector-borne diseases and enhance global health resilience.
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Affiliation(s)
- E Abbasi
- Faculty of Public Health, Department of Biology and Vector Control, Shiraz University of Medical Sciences, Zand Street, JGHF+XFG, Shiraz 3761833650, Fars Province, Iran
- Department of Medical Entomology and Vector Control, School of Health, Shiraz University of Medical Sciences, Shiraz 3761833650, Iran
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8
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Fay RL, Cruz-Loya M, Maffei JG, Mordecai EA, Ciota AT. Temperature influences West Nile virus evolution and adaptation. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2025:2025.02.28.640855. [PMID: 40093049 PMCID: PMC11908156 DOI: 10.1101/2025.02.28.640855] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 03/19/2025]
Abstract
West Nile virus (WNV), the most common mosquito-borne disease in the continental U.S., is vectored by Culex spp. mosquitoes. Since its introduction to New York State (NYS) in 1999, WNV has become endemic. NYS temperatures have risen by 0.14°C per decade since 1900, with larger increases linked to higher WNV transmission. Using surveillance and sequencing data, we find a significant correlation between rising temperatures, increased WNV genetic diversity, and higher prevalence. Given the experimentally demonstrated role of temperature influencing WNV fitness, we hypothesized that contemporary strains should exhibit greater fitness in mosquitoes at higher temperatures compared to historic strains. To test this, we analyzed genetically distinct WNV strains from mosquitoes collected during recent warm summers (2017 and 2018) and cooler historic summers (2003 and 2004). Assessing Culex pipiens vector competence and calculating the relative R₀ at 20°C, 24°C, and 28°C, we found that contemporary strains exhibit higher transmission potential at increased temperatures. Our results show that contemporary WNV strains possess greater phenotypic and genotypic diversity, facilitating the emergence of strains with enhanced transmission potential in a warming climate.
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9
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Heidecke J, Wallin J, Fransson P, Singh P, Sjödin H, Stiles PC, Treskova M, Rocklöv J. Uncovering temperature sensitivity of West Nile virus transmission: Novel computational approaches to mosquito-pathogen trait responses. PLoS Comput Biol 2025; 21:e1012866. [PMID: 40163523 PMCID: PMC11981226 DOI: 10.1371/journal.pcbi.1012866] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/23/2024] [Revised: 04/09/2025] [Accepted: 02/10/2025] [Indexed: 04/02/2025] Open
Abstract
Temperature influences the transmission of mosquito-borne pathogens with significant implications for disease risk under climate change. Mathematical models of mosquito-borne infections rely on functions that capture mosquito-pathogen interactions in response to temperature to accurately estimate transmission dynamics. For deriving these functions, experimental studies provide valuable data on the temperature sensitivity of mosquito life-history traits and pathogen transmission. However, the scarcity of experimental data and inconsistencies in methodologies for analysing temperature responses across mosquito species, pathogens, and experiments present major challenges. Here, we introduce a new approach to address these challenges. We apply this framework to study the thermal biology of West Nile virus (WNV). We reviewed existing experimental studies, obtaining temperature responses for eight mosquito-pathogen traits across 15 mosquito species. Using these data, we employed Bayesian hierarchical models to estimate temperature response functions for each trait and their variation between species and experiments. We incorporated the resulting functions into mathematical models to estimate the temperature sensitivity of WNV transmission, focusing on six mosquito species of the genus Culex. Our study finds a general optimal transmission temperature around 24°C among Culex species with only small species-specific deviations. We demonstrate that differing mechanistic assumptions underlying published mosquito population models result in temperature optima estimates that differ by up to 3°C. Additionally, we find substantial variability between trait temperature responses across experiments on the same species, possibly indicating significant intra-species variation in trait performance. We identify mosquito biting rate, lifespan, and egg viability as priorities for future experiments, as they strongly influence estimates of temperature limits, optima, and overall uncertainty in transmission suitability. Experimental studies on vector competence traits are also essential, because limited data on these currently require model simplifications. These data would enhance the accuracy of our estimates, critical for anticipating future shifts in WNV risk under climate change.
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Affiliation(s)
- Julian Heidecke
- Interdisciplinary Center for Scientific Computing, Heidelberg University, Heidelberg, Germany,
- Heidelberg Institute of Global Health, Heidelberg University, Heidelberg, Germany
| | - Jonas Wallin
- Department of statistics, Lund university, Lund, Sweden
| | - Peter Fransson
- Interdisciplinary Center for Scientific Computing, Heidelberg University, Heidelberg, Germany,
| | - Pratik Singh
- Interdisciplinary Center for Scientific Computing, Heidelberg University, Heidelberg, Germany,
| | - Henrik Sjödin
- Heidelberg Institute of Global Health, Heidelberg University, Heidelberg, Germany
- Department of public health and clinical medicine, Section of sustainable health, Umeå university, Umeå, Sweden
| | | | - Marina Treskova
- Interdisciplinary Center for Scientific Computing, Heidelberg University, Heidelberg, Germany,
- Heidelberg Institute of Global Health, Heidelberg University, Heidelberg, Germany
| | - Joacim Rocklöv
- Interdisciplinary Center for Scientific Computing, Heidelberg University, Heidelberg, Germany,
- Heidelberg Institute of Global Health, Heidelberg University, Heidelberg, Germany
- Department of public health and clinical medicine, Section of sustainable health, Umeå university, Umeå, Sweden
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10
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Kribs CM. Estimating per-infection cost and burden for dengue and Zika as a function of antibody-dependent enhancement. PLoS Negl Trop Dis 2025; 19:e0012876. [PMID: 40014622 PMCID: PMC11906165 DOI: 10.1371/journal.pntd.0012876] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/08/2024] [Revised: 03/13/2025] [Accepted: 01/28/2025] [Indexed: 03/01/2025] Open
Abstract
The complex immune interactions produced by the tetravalent dengue vaccine Dengvaxia have foregrounded the important role of antibody-dependent enhancement (ADE) in dengue infection. Some evidence exists that ADE may extend beyond the four dengue serotypes to Zika, a closely related flavivirus transmitted by the same mosquito species as dengue, and may also account for the increased severity of some cases. Estimates of the public health impact of dengue vaccination may then need to include its effects on the transmission of Zika in addition to dengue. This study gathers primary references to build estimates of per-case economic cost and disease burden for dengue and Zika infection with and without ADE in the ten countries where clinical trials were held for Dengvaxia, under the hypothesis that severe outcomes are associated with ADE of disease. From these estimates, per-infection weighted averages are developed (without assumptions on transmission dynamics or case totals) which will facilitate population-level estimates of the potential impact of dengue vaccination on a dual outbreak using mathematical modeling. Results estimate that ADE amplifies the per-case toll of dengue by a factor of 2-16 but increases that of a Zika case by more than two orders of magnitude due to the greater risk of severe consequences. As expected, dengue vaccination affects per-infection dengue toll much more when high prior dengue seropositivity involves a different serotype than the one(s) circulating, but that same high dengue seropositivity makes vaccination exacerbate Zika toll less.
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Affiliation(s)
- Christopher M. Kribs
- Departments of Mathematics and Teacher & Administrator Preparation, University of Texas at Arlington, Arlington, Texas, United States of America
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11
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Azerigyik FA, Cagle SM, Wilson WC, Mitzel DN, Kading RC. The Temperature-Associated Effects of Rift Valley Fever Virus Infections in Mosquitoes and Climate-Driven Epidemics: A Review. Viruses 2025; 17:217. [PMID: 40006972 PMCID: PMC11860320 DOI: 10.3390/v17020217] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/28/2024] [Revised: 12/31/2024] [Accepted: 01/29/2025] [Indexed: 02/27/2025] Open
Abstract
Rift Valley fever virus (RVFV) is a mosquito-borne zoonotic disease within the genus Phlebovirus. Symptoms of the disease in animals range from moderate to severe febrile illness, which significantly impacts the livestock industry and causes severe health complications in humans. Similar to bunyaviruses in the genus Orthobunyavirus transmitted by mosquitoes, RVFV progression is dependent on the susceptibility of the physical, cellular, microbial, and immune response barriers of the vectors. These barriers, shaped by the genetic makeup of the mosquito species and the surrounding environmental temperature, exert strong selective pressure on the virus, affecting its replication, evolution, and spread. The changing climate coupled with the aforementioned bottlenecks are significant drivers of RVF epidemics and expansion into previously nonendemic areas. Despite the link between microclimatic changes and RVF outbreaks, there is still a dearth of knowledge on how these temperature effects impact RVF transmission and vector competence and virus persistence during interepidemic years. This intricate interdependence between the virus, larval habitat temperatures, and vector competence necessitates increased efforts in addressing RVFV disease burden. This review highlights recent advancements made in response to shifting demographics, weather patterns, and conveyance of RVFV. Additionally, ongoing studies related to temperature-sensitive variations in RVFV-vector interactions and knowledge gaps are discussed.
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Affiliation(s)
- Faustus A. Azerigyik
- Center for Vector-Borne Infectious Diseases, Department of Microbiology, Immunology & Pathology, Colorado State University, Fort Collins, CO 80523, USA; (F.A.A.); (S.M.C.)
| | - Shelby M. Cagle
- Center for Vector-Borne Infectious Diseases, Department of Microbiology, Immunology & Pathology, Colorado State University, Fort Collins, CO 80523, USA; (F.A.A.); (S.M.C.)
| | - William C. Wilson
- Foreign Arthropod-Borne Animal Diseases Research Unit, Agricultural Research Service, United States Department of Agriculture, 1515 College Ave., Manhattan, KS 66502, USA; (W.C.W.); (D.N.M.)
| | - Dana N. Mitzel
- Foreign Arthropod-Borne Animal Diseases Research Unit, Agricultural Research Service, United States Department of Agriculture, 1515 College Ave., Manhattan, KS 66502, USA; (W.C.W.); (D.N.M.)
| | - Rebekah C. Kading
- Center for Vector-Borne Infectious Diseases, Department of Microbiology, Immunology & Pathology, Colorado State University, Fort Collins, CO 80523, USA; (F.A.A.); (S.M.C.)
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12
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Dinesh A, Bommu SPR, Balakrishnan A, Borode M, Bardeskar J, Ramalingam A, Mall A, Pardeshi G. Mapping the Outbreaks of Dengue and Chikungunya and Their Syndemic in India: A Comprehensive Analysis Over the Past Decade Utilizing the Data From the Integrated Disease Surveillance Programme (IDSP). Cureus 2025; 17:e77193. [PMID: 39925612 PMCID: PMC11806968 DOI: 10.7759/cureus.77193] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 01/09/2025] [Indexed: 02/11/2025] Open
Abstract
BACKGROUND This study examines the geographic distribution, temporal trends, and syndemic interactions between dengue and chikungunya outbreaks in India from 2014 to 2023, using data from the Integrated Disease Surveillance Programme (IDSP). Understanding trends offers critical insights to enhance public health responses to co-occurring vector-borne diseases. OBJECTIVES The study analyzes the trends, geographic distribution, and syndemic interactions between dengue and chikungunya. It highlights patterns, high-burden areas, and seasonal dynamics to inform public health interventions for mitigating the dual burden. METHODS This secondary data analysis used IDSP records from January 2014 to December 2023. Temporal trends in outbreaks were analyzed, and districts were categorized by severity through spatial mapping and bivariate analysis, employing statistical quartiles to assess the co-occurrence and syndemic nature of dengue and chikungunya. RESULTS Dengue outbreaks increased significantly from 2014 to 2017, peaking at 175 outbreaks, followed by fluctuations until a peak of 200 outbreaks in 2023. In contrast, chikungunya outbreaks peaked in 2017 at 77 outbreaks and subsequently declined to 19 outbreaks by 2023. Geographic analysis indicated a high dengue burden in districts such as East Siang (Arunachal Pradesh), Birbhum (West Bengal), and Pune (Maharashtra), while chikungunya was most severe in Thanjavur, Theni, and Vellore (Tamil Nadu). A bivariate choropleth analysis identified regions with significant syndemic, such as Pune (Maharashtra), Tumkur (Karnataka), and Kamrup (Assam), which were classified as high-high. Additional districts such as Sangli and Satara (Maharashtra) were categorized as high-moderate, while Puducherry and Junagadh (Gujarat) were noted as moderate-high for dengue and chikungunya, respectively. CONCLUSIONS The findings underscore significant variability in dengue and chikungunya syndemic across India, highlighting regions with severe dual burden. Enhanced surveillance for close watch on syndemic occurrence and its impact needs to be studied, which is essential to reduce both the incidence and study its compounded public health impacts.
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Affiliation(s)
- Asokan Dinesh
- Department of Community Medicine, Grant Government Medical College and Sir Jamshedjee Jeejeebhoy (JJ) Group of Hospitals, Mumbai, IND
| | - Siva Prasad Reddy Bommu
- Department of Community Medicine, Grant Government Medical College and Sir Jamshedjee Jeejeebhoy (JJ) Group of Hospitals, Mumbai, IND
| | - Aishwarya Balakrishnan
- Department of Community Medicine, Grant Government Medical College and Sir Jamshedjee Jeejeebhoy (JJ) Group of Hospitals, Mumbai, IND
| | - Minal Borode
- Department of Community Medicine, Grant Government Medical College and Sir Jamshedjee Jeejeebhoy (JJ) Group of Hospitals, Mumbai, IND
| | - Joyce Bardeskar
- Department of Community Medicine, Grant Government Medical College and Sir Jamshedjee Jeejeebhoy (JJ) Group of Hospitals, Mumbai, IND
| | - Ajith Ramalingam
- Department of Community Medicine, Grant Government Medical College and Sir Jamshedjee Jeejeebhoy (JJ) Group of Hospitals, Mumbai, IND
| | - Anjali Mall
- Department of Community Medicine, Grant Government Medical College and Sir Jamshedjee Jeejeebhoy (JJ) Group of Hospitals, Mumbai, IND
| | - Geeta Pardeshi
- Department of Community Medicine, Grant Government Medical College and Sir Jamshedjee Jeejeebhoy (JJ) Group of Hospitals, Mumbai, IND
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13
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Brettell LE, Hoque AF, Joseph TS, Dhokiya V, Hornett EA, Hughes GL, Heinz E. Mosquitoes Reared in Nearby Insectaries at the Same Institution Have Significantly Divergent Microbiomes. Environ Microbiol 2025; 27:e70027. [PMID: 39779320 PMCID: PMC11711076 DOI: 10.1111/1462-2920.70027] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/06/2024] [Revised: 11/28/2024] [Accepted: 12/03/2024] [Indexed: 01/11/2025]
Abstract
The microbiome influences critical aspects of mosquito biology and variations in microbial composition can impact the outcomes of laboratory studies. To investigate how biotic and abiotic conditions in an insectary affect the composition of the mosquito microbiome, a single cohort of Aedes aegypti eggs was divided into three batches and transferred to three different climate-controlled insectaries within the Liverpool School of Tropical Medicine. The bacterial microbiome composition was compared as mosquitoes developed, the microbiome of the mosquitoes' food sources was characterised, environmental conditions over time in each insectary were measured, and mosquito development and survival were recorded. While developmental success was similar across all three insectaries, differences in microbiome composition were observed between mosquitoes from each insectary. Environmental conditions and bacterial input via food sources varied between insectaries, potentially contributing to the observed differences in microbiome composition. At both adult and larval stages, specific members of the mosquito microbiome were associated with particular insectaries; the insectary with less stable and cooler conditions resulted in a slower pupation rate and higher diversity of the larval microbiome. These findings underscore that even minor inconsistencies in rearing conditions can affect the composition of the mosquito microbiome, which may influence experimental outcomes.
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Affiliation(s)
- Laura E. Brettell
- Department of Vector BiologyLiverpool School of Tropical MedicineLiverpoolUK
- School of Science, Engineering and EnvironmentUniversity of SalfordManchesterUK
| | - Ananya F. Hoque
- Department of Vector BiologyLiverpool School of Tropical MedicineLiverpoolUK
- The Roslin Institute, Royal (Dick) School of Veterinary StudiesThe University of EdinburghMidlothianUK
| | - Tara S. Joseph
- Department of Vector BiologyLiverpool School of Tropical MedicineLiverpoolUK
- Department of Tropical Disease Biology, Centre for Neglected Tropical DiseasesLiverpool School of Tropical MedicineLiverpoolUK
| | - Vishaal Dhokiya
- Department of Vector BiologyLiverpool School of Tropical MedicineLiverpoolUK
- Department of Tropical Disease Biology, Centre for Neglected Tropical DiseasesLiverpool School of Tropical MedicineLiverpoolUK
| | - Emily A. Hornett
- Department of Vector BiologyLiverpool School of Tropical MedicineLiverpoolUK
- Department of Tropical Disease Biology, Centre for Neglected Tropical DiseasesLiverpool School of Tropical MedicineLiverpoolUK
- Department of Evolution, Ecology and BehaviourUniversity of LiverpoolLiverpoolUK
| | - Grant L. Hughes
- Department of Vector BiologyLiverpool School of Tropical MedicineLiverpoolUK
- Department of Tropical Disease Biology, Centre for Neglected Tropical DiseasesLiverpool School of Tropical MedicineLiverpoolUK
| | - Eva Heinz
- Department of Vector BiologyLiverpool School of Tropical MedicineLiverpoolUK
- Department of Clinical SciencesLiverpool School of Tropical MedicineLiverpoolUK
- Strathclyde Institute of Pharmacy and Biomedical SciencesUniversity of StrathclydeGlasgowUK
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14
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Thakur CK, Adhikari S, Dhimal M. Climate-driven dengue fever outbreaks in Nepal: Trends, challenges, and strategies. World J Virol 2024; 13:95450. [PMID: 39722754 PMCID: PMC11551688 DOI: 10.5501/wjv.v13.i4.95450] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/10/2024] [Revised: 09/07/2024] [Accepted: 09/30/2024] [Indexed: 10/18/2024] Open
Abstract
Dengue fever (DF) has become a major public health concern in Nepal, with increasing outbreaks in recent years. Transmitted by Aedes mosquitoes, this climate-sensitive viral disease presents a significant challenge for healthcare providers and policymakers. Since 2004, Nepal has experienced a sharp increase in DF cases, peaking in 2022 with 54784 cases and 88 deaths. The surge, driven mainly by serotypes 1, 2, and 3, is exacerbated by climate change, which prolongs mosquito breeding seasons due to warmer temperatures and increased rainfall. This trend has even impacted previously unaffected hilly regions. Effective dengue control strategies must focus on climate change adaptation, strengthening healthcare system reinforcement, raising public awareness, and enhancing vector control measures. Government initiatives, like the national dengue control program, play a critical role, but research and community engagement are also vital for prevention and early detection. Integrating climate resilience into public health efforts is essential to reducing the dengue burden in Nepal.
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Affiliation(s)
- Chandan Kumar Thakur
- Clinical Microbiology, Karnali Academy of Health Sciences, Jumla 21200, Karnali, Nepal
| | - Samita Adhikari
- Hospital Infection Control, Nepal Mediciti Hospital, Lalitpur 44700, Bagmati, Nepal
| | - Meghnath Dhimal
- Research Section, Nepal Health Research Council, Kathmandu 44600, Bagmati, Nepal
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15
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Turner EA, Clark SD, Peña-García VH, Christofferson RC. Investigating the Effects of Microclimate on Arboviral Kinetics in Aedes aegypti. Pathogens 2024; 13:1105. [PMID: 39770364 PMCID: PMC11728849 DOI: 10.3390/pathogens13121105] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/11/2024] [Revised: 12/02/2024] [Accepted: 12/09/2024] [Indexed: 01/16/2025] Open
Abstract
Aedes aegypti are indoor-dwelling vectors of many arboviruses, including Zika (ZIKV) and chikungunya (CHIKV). The dynamics of these viruses within the mosquito are known to be temperature-dependent, and models that address risk and predictions of the transmission efficiency and patterns typically use meteorological temperature data. These data do not differentiate the temperatures experienced by mosquitoes in different microclimates, such as indoor vs. outdoor. Using temperature data collected from Neiva Colombia, we investigated the impact of two microclimate temperature profiles on ZIKV and CHIKV infection dynamics in Ae. aegypti. We found that the vector mortality was not significantly impacted by the difference in temperature profiles. Further, we found that the infection and dissemination rates were largely unaffected, with only ZIKV experiencing a significant increase in infection at outdoor temperatures at 21 days post-infection (dpi). Further, there was a significant increase in viral titers in the abdomens of ZIKV-infected mosquitoes at 21 dpi. With CHIKV, there was a significant titer difference in the abdomens of mosquitoes at both 7 and 14 dpi. While there were differences in vector infection kinetics that were not statistically significant, we developed a simple stochastic SEIR-SEI model to determine if the observed differences might translate to notable differences in simulated outbreaks. With ZIKV, while the probability of secondary transmission was high (>90%) under both microenvironmental scenarios, there was often only one secondary case. However, CHIKV differences between microenvironments were more prominent. With over 90% probability of secondary transmission, at indoor conditions, the peak of transmission was higher (over 850 cases) compared to the outdoor conditions (<350 cases). Further, the time-to-peak for indoor was 130 days compared to 217 days for outdoor scenarios. Further investigations into microenvironmental conditions, including temperature, may be key to increasing our understanding of the nuances of CHIKV and ZIKV vectorial capacity, epidemiology, and risk assessment, especially as it affects other aspects of transmission, such as biting rate. Overall, it is critical to understand the variability of how extrinsic factors affect transmission systems, and these data add to the growing catalog of knowledge of how temperature affects arboviral systems.
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Affiliation(s)
- Erik A Turner
- Department of Pathobiological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
| | - Samantha D Clark
- Department of Pathobiological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
| | - Víctor Hugo Peña-García
- Department of Biology, Stanford University, Stanford, CA 94305, USA
- School of Medicine, Stanford University, Stanford, CA 94305, USA
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16
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Lühken R, Rauhöft L, Pluskota B, Lange U, Helms M, Becker N, Schmidt-Chanasit J, Kuhn C, Tannich E, Jansen S, Heitmann A. High vector competence for chikungunya virus but heavily reduced locomotor activity of Aedes albopictus from Germany at low temperatures. Parasit Vectors 2024; 17:502. [PMID: 39633401 PMCID: PMC11619113 DOI: 10.1186/s13071-024-06594-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/11/2024] [Accepted: 11/21/2024] [Indexed: 12/07/2024] Open
Abstract
BACKGROUND The incidence of human infections caused by arthropod-borne viruses, such as the chikungunya virus (CHIKV), has increased globally due to a number of factors, such as climate change and globalization. The exotic mosquito species Aedes albopictus is a significant vector for CHIKV, raising concerns about its transmission potential in temperate regions, including Central Europe. We have therefore investigated the vector competence of Ae. albopictus for CHIKV at constant and fluctuating temperatures between 15 °C and 24 °C to assess the transmission risk in Europe. METHODS Aedes albopictus mosquitoes were reared and artificially infected with CHIKV. Infection rates and transmission efficiencies (TEs) were determined after 14 days of incubation at constant and fluctuating (± 5 °C) mean temperatures of 15 °C, 18 °C, 21 °C and 24 °C. In addition, mosquito locomotor activity was measured under the same fluctuating temperature conditions. A risk map for CHIKV transmission in Europe was generated combining temperature data and the current distribution of Ae. albopictus. RESULTS CHIKV transmission was observed at all tested temperatures. The highest TEs were recorded at fluctuating temperatures of 18 °C (54.3%) and 21 °C (58.6%), while the lowest TE was observed at a constant temperature of 15 °C (5.6%). TEs at fluctuating temperatures of 15 °C and 24 °C were the same (32.5%). Mosquito activity showed a nocturnal unimodal activity pattern with a peak during the start of the scotophase (hour 20). The proportion of active mosquitoes per hour increased with temperature and was nearly zero at 15 °C. The risk map indicated that regions in Southern and Central Europe, including recently invaded areas north of the Alps, have temperatures theoretically allowing CHIKV transmission for at least some days per year. CONCLUSIONS While CHIKV can be transmitted by Ae. albopictus at 15 °C, the activity of this mosquito is strongly decreased at this temperature, likely reducing the transmission risk. These findings emphasize the importance of considering both vector competence and mosquito activity when assessing the risk of arbovirus transmission in temperate regions. Further studies are needed to validate these laboratory findings under field conditions.
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Affiliation(s)
- Renke Lühken
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany.
| | - Leif Rauhöft
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
| | - Björn Pluskota
- Kommunale Aktionsgemeinschaft zur Bekämpfung der Schnakenplage (KABS E.V.), Speyer, Germany
| | - Unchana Lange
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
| | - Michelle Helms
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
| | - Norbert Becker
- Institute for Dipterology (IfD), Speyer, Germany
- Center for Organismal Studies (COS), University of Heidelberg, Heidelberg, Germany
| | - Jonas Schmidt-Chanasit
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
- Faculty of Mathematics, Informatics and Natural Sciences, Universität Hamburg, Hamburg, Germany
| | - Carola Kuhn
- German Environment Agency (UBA), Berlin, Germany
| | - Egbert Tannich
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
| | - Stephanie Jansen
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
- Faculty of Mathematics, Informatics and Natural Sciences, Universität Hamburg, Hamburg, Germany
| | - Anna Heitmann
- Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany
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17
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Montenegro D, Cortés-Cortés G, Balbuena-Alonso MG, Warner C, Camps M. Wolbachia-based emerging strategies for control of vector-transmitted disease. Acta Trop 2024; 260:107410. [PMID: 39349234 PMCID: PMC11637914 DOI: 10.1016/j.actatropica.2024.107410] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/03/2024] [Revised: 09/21/2024] [Accepted: 09/23/2024] [Indexed: 10/02/2024]
Abstract
Dengue fever is a mosquito-transmitted disease of great public health importance. Dengue lacks adequate vaccine protection and insecticide-based methods of mosquito control are proving increasingly ineffective. Here we review the emerging use of mosquitoes transinfected with the obligate intracellular bacterium Wolbachia pipientis for vector control. Wolbachia often induces cytoplasmic incompatibility in its mosquito hosts, resulting in infertile progeny between an infected male and an uninfected female. Wolbachia infection also suppresses the replication of pathogens in the mosquito, a process known as "pathogen blocking". Two strategies have emerged. The first one releases Wolbachia carriers (both male and female) to replace the wild mosquito population, a process driven by cytoplasmic incompatibility and that becomes irreversible once a threshold is reached. This suppresses disease transmission mainly by pathogen blocking and frequently requires a single intervention. The second strategy floods the field population with an exclusively male population of Wolbachia-carrying mosquitoes to generate infertile hybrid progeny. In this case, transmission suppression depends largely on decreasing the population density of mosquitoes driven by infertility and requires continued mosquito release. The efficacy of both Wolbachia-based approaches has been conclusively demonstrated by randomized and non-randomized studies of deployments across the world. However, results conducted in one setting cannot be directly or easily extrapolated to other settings because dengue incidence is highly affected by the conditions into which the mosquitoes are released. Compared to traditional vector control methods, Wolbachia-based approaches are much more environmentally friendly and can be effective in the medium/long term. On the flip side, they are much more complex and cost-intensive operations, requiring a substantial investment, infrastructure, trained personnel, coordination between agencies, and community engagement. Finally, we discuss recent evidence suggesting that the release of Wolbachia-transinfected mosquitoes has a moderate potential risk of spreading potentially dangerous genes in the environment.
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Affiliation(s)
- Diego Montenegro
- Corporación Innovation Hub, Monteria 230001, Colombia; Department of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA 95064, USA; Grupo de Investigación: Salud y Tecnología 4.0. Fundación Chilloa, Santa Marta 470001, Colombia
| | - Gerardo Cortés-Cortés
- Department of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA 95064, USA; Posgrado en Microbiología, Centro de Investigaciones en Ciencias Microbiológicas, Instituto de Ciencias de la Benemérita Universidad Autónoma de Puebla, Ciudad Universitaria, San Manuel, Puebla 72570, Mexico
| | - María Guadalupe Balbuena-Alonso
- Department of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA 95064, USA; Posgrado en Microbiología, Centro de Investigaciones en Ciencias Microbiológicas, Instituto de Ciencias de la Benemérita Universidad Autónoma de Puebla, Ciudad Universitaria, San Manuel, Puebla 72570, Mexico
| | - Caison Warner
- Department of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA 95064, USA
| | - Manel Camps
- Department of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA 95064, USA.
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Doeurk B, Marcombe S, Maquart PO, Boyer S. Review of dengue vectors in Cambodia: distribution, bionomics, vector competence, control and insecticide resistance. Parasit Vectors 2024; 17:424. [PMID: 39385238 PMCID: PMC11462738 DOI: 10.1186/s13071-024-06481-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/11/2024] [Accepted: 09/03/2024] [Indexed: 10/12/2024] Open
Abstract
BACKGROUND Dengue fever is one of the most prevalent mosquito-borne diseases in Cambodia. Until now, no specific vaccine nor antiviral treatment exists the virus causing Dengue fever. Consequently, its prevention relies only on vector control strategies. However, efficient vector control in turn relies on a good knowledge of the biology of the vector species. Therefore, this study aims to provide the first review of the distribution, ecology, meteorological impacts, trophic behavior, vector competence, vector control and insecticide resistance of dengue vector species in Cambodia. METHODS A systematic search of the Google Scholar and PubMed databases was conducted for relevant published articles. Of the 610 published articles originally identified, 70 articles were ultimately selected for inclusion in this review. We also included new data from unpublished research conducted in Cambodia between 2017 and 2023 related to dengue vector bionomics. RESULTS Eleven Aedes (Stegomyia) mosquito species have been recorded in Cambodia, including a new species described in 2024. Four species are associated with dengue virus transmission, among which Aedes aegypti and Ae. albopictus are the main vectors and Ae. malayensis and Ae. scutellaris are considered to be potential vectors. Aedes aegypti and Ae. albopictus are present in all provinces of Cambodia. Aedes albopictus shows a preference for forest, rural and suburban areas, while Ae. aegypti is mostly found in urban and suburban areas. The distribution of these two species is also influenced by meteorological factors, seasonality and the availability of breeding habitats and blood meals. Both species are predominant during the rainy season, and their respective density is impacted by precipitation and temperature. Aedes aegypti is characterized as anthropophilic, while Ae. albopictus exhibits zooanthropophilic behavior, and both species have been observed to be predominantly diurnal. In addition, they were found to be highly resistant to the insecticides used in Cambodia for their control, such as temephos for larvae and deltamethrin and permethrin for adult mosquitoes. CONCLUSIONS This review provides extensive and important knowledge on dengue vectors in Cambodia. This knowledge is derived not only from published research articles but also from many recent studies in Cambodia on the bionomics of dengue vector species. The review provides valuable information for use by public health authorities on dengue virus transmission and to develop better vector control strategies in the country.
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Affiliation(s)
- Bros Doeurk
- Medical and Veterinary Entomology Unit, Institut Pasteur du Cambodge, PO Box 983, Phnom Penh, Cambodia.
| | | | - Pierre-Olivier Maquart
- Medical and Veterinary Entomology Unit, Institut Pasteur du Cambodge, PO Box 983, Phnom Penh, Cambodia
- IRD, UMR 247 Evolution, Génome, Comportement, Ecologie,, Université Paris-Saclay, Gif-Sur-Yvette, France
| | - Sébastien Boyer
- Medical and Veterinary Entomology Unit, Institut Pasteur du Cambodge, PO Box 983, Phnom Penh, Cambodia
- Ecology and Emergence of Arthropod-Borne Diseases, Institut Pasteur, Paris, France
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Hall JM, Tiatragul S, Turner MK, Warner DA. Within the optimal thermal range, temperature fluctuations with similar means have little effect on offspring phenotypes: A comparison of two approaches that simulate natural nest conditions. J Therm Biol 2024; 125:103949. [PMID: 39306971 DOI: 10.1016/j.jtherbio.2024.103949] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/19/2024] [Revised: 07/01/2024] [Accepted: 07/28/2024] [Indexed: 11/25/2024]
Abstract
Temperature influences nearly every aspect of organismal function. Because aspects of global change such as urbanization and climate change influence temperature, researchers must consider how altering thermal regimes will impact biodiversity across the planet. To do so, they often measure temperature in natural and/or human-modified habitats, replicate those temperatures in laboratory experiments to understand organismal responses, and make predictions under models of future change. Consequently, accurately representing temperature in the laboratory is an important concern, yet few studies have assessed the consequences of simulating thermal conditions in different ways. We used nest temperatures for two urban-dwelling, invasive lizards (Anolis sagrei and A. cristatellus) to create two egg incubation treatments in the laboratory. Like most studies of thermal developmental plasticity, we created daily repeating thermal fluctuations; however, we used different methods to create temperature treatments that differed in the magnitude and breadth of thermal cycles, and then evaluated the effects of these different approaches on embryo development and hatchling phenotypes. Additionally, we measured embryo heart rate, a proxy for metabolism, across temperature to understand the immediate effects of treatments. We found that treatments had minimal effect on phenotypes likely because temperatures were within the optimal thermal range for each species and were similar in mean temperature. We conclude that slight differences in thermal treatments may be unimportant so long as temperatures are within a range appropriate for development, and we make several recommendations for future studies of developmental plasticity.
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Affiliation(s)
- Joshua M Hall
- Department of Biological Sciences, Auburn University, Auburn, AL, 36849, USA; Department of Biology, Tennessee Tech University, Cookeville, TN, 38505, USA.
| | - Sarin Tiatragul
- Department of Biological Sciences, Auburn University, Auburn, AL, 36849, USA; Division of Ecology & Evolution, Research School of Biology, The Australian National University, Canberra, ACT, 2601, Australia
| | - Mallory K Turner
- Department of Biological Sciences, Auburn University, Auburn, AL, 36849, USA
| | - Daniel A Warner
- Department of Biological Sciences, Auburn University, Auburn, AL, 36849, USA
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Souza CDFD, Nascimento RPDS, Bezerra-Santos M, Armstrong ADC, Gomes OV, Nicácio JM, Júnior JVJS, Carmo RFD. Space-time dynamics of the dengue epidemic in Brazil, 2024: an insight for decision making. BMC Infect Dis 2024; 24:1056. [PMID: 39333905 PMCID: PMC11430439 DOI: 10.1186/s12879-024-09813-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/20/2024] [Accepted: 08/27/2024] [Indexed: 09/30/2024] Open
Abstract
BACKGROUND Dengue is a vector-borne viral infection caused by the dengue virus transmitted to humans primarily by Aedes aegypti. The year 2024 has been a historic year for dengue in Brazil, with the highest number of probable cases ever registered. Herein, we analyze the temporal trend and spatio-temporal dynamics of dengue cases in Brazil during the first nine epidemiological weeks (EW) of 2024. METHODS This is an ecological study, including all probable cases of dengue in Brazil during the period, carried out in two steps: time series analysis to assess the temporal trend and spatial analysis to identify high-risk clusters. RESULTS 1,345,801 probable cases of dengue were reported. The regions with the highest increasing trend were the Northeast with an average epidemiologic week percent change (AEPC) of 52.4 (95% CI: 45.5-59.7; p < 0.001) and the South with 35.9 (95% CI: 27.7-44.5; p < 0.001). There was a statistically significant increasing trend in all states, except Acre (AEPC = -4.1; 95% CI: -16.3-10; p = 0.55), Amapá (AEPC = 1.3; 95% CI: -16.2-22.3; p = 0.9) and Espírito Santo (AEPC = 8.9; 95% CI: -15.7-40.6; p = 0.5). The retrospective space-time analysis showed a cluster within the Northeast, Central-West and Southeast regions, with a radius of 515.3 km, in which 1,267 municipalities and 525,324 of the cases were concentrated (RR = 6.3; p < 0.001). Regarding the spatial variation of the temporal trend, 21 risk areas were found, all of them located in Southeast or Central-West states. The area with the highest relative risk was Minas Gerais state, where 5,748 cases were concentrated (RR = 8.1; p < 0.001). Finally, a purely spatial analysis revealed 25 clusters, the one with the highest relative risk being composed of two municipalities in Acre (RR = 6.9; p < 0.001). CONCLUSIONS We described a detailed temporal-spatial analysis of dengue cases in the first EWs of 2024 in Brazil, which were mainly concentrated in the Southeast and Central-West regions. Overall, it is recommended that governments adopt public policies to control the the vector population in high-risk areas, as well as to prevent the spread of dengue fever to other areas of Brazil.
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Affiliation(s)
- Carlos Dornels Freire de Souza
- College of Medicine, Federal University of the São Francisco Valley (UNIVASF), José de Sá Maniçoba, Centro, Arapiraca, Petrolina, Pernambuco, Alagoas, 56304-917, Brazil.
- Research CNPq N2, Postgraduate Program in Family Health, Oswaldo Cruz Foundation (Fiocruz), Rio de Janeiro, Brazil.
| | - Rafael Pedro de Souza Nascimento
- College of Medicine, Federal University of the São Francisco Valley (UNIVASF), José de Sá Maniçoba, Centro, Arapiraca, Petrolina, Pernambuco, Alagoas, 56304-917, Brazil
| | - Márcio Bezerra-Santos
- College of Medicine, Federal University of Alagoas (UFAL), Arapiraca, Alagoas, Brazil
| | - Anderson da Costa Armstrong
- College of Medicine, Federal University of the São Francisco Valley (UNIVASF), José de Sá Maniçoba, Centro, Arapiraca, Petrolina, Pernambuco, Alagoas, 56304-917, Brazil
| | - Orlando Vieira Gomes
- College of Medicine, Federal University of the São Francisco Valley (UNIVASF), José de Sá Maniçoba, Centro, Arapiraca, Petrolina, Pernambuco, Alagoas, 56304-917, Brazil
| | - Jandir Mendonça Nicácio
- College of Medicine, Federal University of the São Francisco Valley (UNIVASF), José de Sá Maniçoba, Centro, Arapiraca, Petrolina, Pernambuco, Alagoas, 56304-917, Brazil
| | - José Valter Joaquim Silva Júnior
- Virology Sector, Department of Preventive Veterinary Medicine, Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Brazil
- Virology Sector, Keizo Asami Institute, Federal University of Pernambuco, Pernambuco, Brazil
- NB3 Neuroimmunology Laboratory, Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Brazil
- Department of Microbiology and Parasitology, Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Brazil
| | - Rodrigo Feliciano do Carmo
- College of Medicine, Federal University of the São Francisco Valley (UNIVASF), José de Sá Maniçoba, Centro, Arapiraca, Petrolina, Pernambuco, Alagoas, 56304-917, Brazil
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Vinauger C, Chandrasegaran K. Context-specific variation in life history traits and behavior of Aedes aegypti mosquitoes. FRONTIERS IN INSECT SCIENCE 2024; 4:1426715. [PMID: 39386346 PMCID: PMC11461241 DOI: 10.3389/finsc.2024.1426715] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 05/02/2024] [Accepted: 08/19/2024] [Indexed: 10/12/2024]
Abstract
Aedes aegypti, the vector for dengue, chikungunya, yellow fever, and Zika, poses a growing global epidemiological risk. Despite extensive research on Ae. aegypti's life history traits and behavior, critical knowledge gaps persist, particularly in integrating these findings across varied experimental contexts. The plasticity of Ae. aegypti's traits throughout its life cycle allows dynamic responses to environmental changes, yet understanding these variations within heterogeneous study designs remains challenging. A critical aspect often overlooked is the impact of using lab-adapted lines of Ae. aegypti, which may have evolved under laboratory conditions, potentially altering their life history traits and behavioral responses compared to wild populations. Therefore, incorporating field-derived populations in experimental designs is essential to capture the natural variability and adaptability of Ae. aegypti. The relationship between larval growing conditions and adult traits and behavior is significantly influenced by the specific context in which mosquitoes are studied. Laboratory conditions may not replicate the ecological complexities faced by wild populations, leading to discrepancies in observed traits and behavior. These discrepancies highlight the need for ecologically relevant experimental conditions, allowing mosquito traits and behavior to reflect field distributions. One effective approach is semi-field studies involving field-collected mosquitoes housed for fewer generations in the lab under ecologically relevant conditions. This growing trend provides researchers with the desired control over experimental conditions while maintaining the genetic diversity of field populations. By focusing on variations in life history traits and behavioral plasticity within these varied contexts, this review highlights the intricate relationship between larval growing conditions and adult traits and behavior. It underscores the significance of transstadial effects and the necessity of adopting study designs and reporting practices that acknowledge plasticity in adult traits and behavior, considering variations due to larval rearing conditions. Embracing such approaches paves the way for a comprehensive understanding of contextual variations in mosquito life history traits and behavior. This integrated perspective enables the synthesis of research findings across laboratory, semi-field, and field-based investigations, which is crucial for devising targeted intervention strategies tailored to specific ecological contexts to combat the health threat posed by this formidable disease vector effectively.
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Affiliation(s)
- Clément Vinauger
- Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA, United States
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22
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Shocket MS, Bernhardt JR, Miazgowicz KL, Orakzai A, Savage VM, Hall RJ, Ryan SJ, Murdock CC. Mean daily temperatures can predict the thermal limits of malaria transmission better than rate summation. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2024:2024.09.20.614098. [PMID: 39386442 PMCID: PMC11463682 DOI: 10.1101/2024.09.20.614098] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Indexed: 10/12/2024]
Abstract
Temperature shapes the distribution, seasonality, and magnitude of mosquito-borne disease outbreaks. Mechanistic models predicting transmission often use mosquito and pathogen thermal responses from constant temperature experiments. However, mosquitoes live in fluctuating environments. Rate summation (nonlinear averaging) is a common approach to infer performance in fluctuating environments, but its accuracy is rarely validated. We measured three mosquito traits that impact transmission (bite rate, survival, fecundity) in a malaria mosquito (Anopheles stephensi) across temperature gradients with three diurnal temperature ranges (0, 9 and 12°C). We compared thermal suitability models with temperature-trait relationships observed under constant temperatures, fluctuating temperatures, and those predicted by rate summation. We mapped results across An. stephenesi's native Asian and invasive African ranges. We found: 1) daily temperature fluctuation significantly altered trait thermal responses; 2) rate summation partially captured decreases in performance near thermal optima, but also incorrectly predicted increases near thermal limits; and 3) while thermal suitability characterized across constant temperatures did not perfectly capture suitability in fluctuating environments, it was more accurate for estimating and mapping thermal limits than predictions from rate summation. Our study provides insight into methods for predicting mosquito-borne disease risk and emphasizes the need to improve understanding of organismal performance under fluctuating conditions.
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Affiliation(s)
- Marta S. Shocket
- Lancaster Environment Centre, Lancaster University, UK
- Department of Geography, University of Florida, USA
- Department of Ecology and Evolutionary Biology, University of California Los Angeles, USA
| | | | | | | | - Van M. Savage
- Department of Ecology and Evolutionary Biology, University of California Los Angeles, USA
| | - Richard J. Hall
- Department of Infectious Diseases, University of Georgia, USA
- Odum School of Ecology, University of Georgia, USA
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23
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Chathurangika P, Premadasa LS, Perera SSN, De Silva K. Determining dengue infection risk in the Colombo district of Sri Lanka by inferencing the genetic parameters of Aedes mosquitoes. BMC Infect Dis 2024; 24:944. [PMID: 39251932 PMCID: PMC11385510 DOI: 10.1186/s12879-024-09878-w] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/10/2024] [Accepted: 09/04/2024] [Indexed: 09/11/2024] Open
Abstract
BACKGROUND For decades, dengue has posed a significant threat as a viral infectious disease, affecting numerous human lives globally, particularly in tropical regions, yet no cure has been discovered. The genetic trait of vector competence in Aedes mosquitoes, which facilitates dengue transmission, is difficult to measure and highly sensitive to environmental changes. METHODS In this study we attempt, for the first time in a non-laboratory setting, to quantify the vector competence of Aedes mosquitoes assuming its homogeneity across both species; aegypti and albopictus and across the four Dengue serotypes. Estimating vector competence in relation to varying rainfall patterns was focused in this study to showcase the changes in this vector trait with respect to environmental variables. We quantify it using an existing mathematical model originally developed for malaria in a Bayesian inferencing setup. We conducted this study in the Colombo district of Sri Lanka where the highest number of human populations are threatened with dengue. Colombo district experiences continuous favorable temperature and humidity levels throughout the year creating ideal conditions for Aedes mosquitoes to thrive and transmit the Dengue disease. Therefore we only used the highly variable and seasonal rainfall as the primary environmental variable as it significantly influences the number of breeding sites and thereby impacting the population dynamics of Aedes. RESULTS Our research successfully deduced vector competence values for the four identified seasons based on Monsoon rainfalls experienced in Colombo within a year. We used dengue data from 2009 - 2022 to infer the estimates. These estimated values have been corroborated through experimental studies documented in the literature, thereby validating the malaria model to estimate vector competence for dengue disease. CONCLUSION Our research findings conclude that environmental conditions can amplify vector competence within specific seasons, categorized by their environmental attributes. Additionally, the deduced vector competence offers compelling evidence that it impacts disease transmission, irrespective of geographical location, climate, or environmental factors.
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Affiliation(s)
- Piyumi Chathurangika
- Research & Development Centre for Mathematical Modeling, Department of Mathematics, Faculty of Science, University of Colombo, 00030, Colombo, Sri Lanka
| | - Lakmini S Premadasa
- International Center for the Advancement of Research and Education (I·CARE), Texas Biomedical Research Institute, San Antonio, 78227, TX, USA
| | - S S N Perera
- Research & Development Centre for Mathematical Modeling, Department of Mathematics, Faculty of Science, University of Colombo, 00030, Colombo, Sri Lanka
| | - Kushani De Silva
- Research & Development Centre for Mathematical Modeling, Department of Mathematics, Faculty of Science, University of Colombo, 00030, Colombo, Sri Lanka.
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Del-Águila-Mejía J, Morilla F, Donado-Campos JDM. A system dynamics modelling and analytical framework for imported dengue outbreak surveillance and risk mapping. Acta Trop 2024; 257:107304. [PMID: 38942132 DOI: 10.1016/j.actatropica.2024.107304] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/22/2024] [Revised: 06/24/2024] [Accepted: 06/25/2024] [Indexed: 06/30/2024]
Abstract
System Dynamics (SD) models have been used to understand complex, multi-faceted dengue transmission dynamics, but a gap persists between research and actionable public health tools for decision-making. Spain is an at-risk country of imported dengue outbreaks, but only qualitative assessments are available to guide public health action and control. We propose a modular SD model combining temperature-dependent vector population, transmission parameters, and epidemiological interactions to simulate outbreaks from imported cases accounting for heterogeneous local climate-related transmission patterns. Under our assumptions, 15 provinces sustain vector populations capable of generating outbreaks from imported cases, with heterogeneous risk profiles regarding seasonality, magnitude and risk window shifting from late Spring to early Autum. Results being relative to given vector-to-human populations allow flexibility when translating outcomes between geographic scales. The model and the framework are meant to serve public health by incorporating transmission dynamics and quantitative-qualitative input to the evidence-based decision-making chain. It is a flexible tool that can easily adapt to changing contexts, parametrizations and epidemiological settings thanks to the modular approach.
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Affiliation(s)
- Javier Del-Águila-Mejía
- Departamento de Medicina Preventiva y Salud Pública y Microbiología, Facultad de Medicina, Universidad Autónoma de Madrid, C. Arzobispo Morcillo, 4, Madrid 28029, Spain; Servicio de Medicina Preventiva, Hospital Universitario de Móstoles, C. Dr. Luis Montes s/n, Madrid, Móstoles 28935, Spain.
| | - Fernando Morilla
- Departamento de Informática y Automática, Universidad Nacional de Educación a Distancia, Juan del Rosal 16, Madrid 28040, Spain
| | - Juan de Mata Donado-Campos
- Departamento de Medicina Preventiva y Salud Pública y Microbiología, Facultad de Medicina, Universidad Autónoma de Madrid, C. Arzobispo Morcillo, 4, Madrid 28029, Spain; Consorcio de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), Instituto de Salud Carlos III, Calle Monforte de Lemos 3-5, Madrid 28029, Spain; Departamento de Medicina, Facultad de Ciencias Biomédicas y de la Salud, Universidad Europea de Madrid, C. Tajo, s/n, Madrid, Villaviciosa de Odón 28670, Spain; Instituto de Investigación Sanitaria del Hospital Universitario La Paz (IdiPAZ), Universidad Autónoma de Madrid, C. Arzobispo Morcillo 4, Madrid 28029, Spain
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Athni TS, Childs ML, Glidden CK, Mordecai EA. Temperature dependence of mosquitoes: Comparing mechanistic and machine learning approaches. PLoS Negl Trop Dis 2024; 18:e0012488. [PMID: 39283940 PMCID: PMC11460681 DOI: 10.1371/journal.pntd.0012488] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/14/2023] [Revised: 10/08/2024] [Accepted: 08/27/2024] [Indexed: 09/21/2024] Open
Abstract
Mosquito vectors of pathogens (e.g., Aedes, Anopheles, and Culex spp. which transmit dengue, Zika, chikungunya, West Nile, malaria, and others) are of increasing concern for global public health. These vectors are geographically shifting under climate and other anthropogenic changes. As small-bodied ectotherms, mosquitoes are strongly affected by temperature, which causes unimodal responses in mosquito life history traits (e.g., biting rate, adult mortality rate, mosquito development rate, and probability of egg-to-adult survival) that exhibit upper and lower thermal limits and intermediate thermal optima in laboratory studies. However, it remains unknown how mosquito thermal responses measured in laboratory experiments relate to the realized thermal responses of mosquitoes in the field. To address this gap, we leverage thousands of global mosquito occurrences and geospatial satellite data at high spatial resolution to construct machine-learning based species distribution models, from which vector thermal responses are estimated. We apply methods to restrict models to the relevant mosquito activity season and to conduct ecologically plausible spatial background sampling centered around ecoregions for comparison to mosquito occurrence records. We found that thermal minima estimated from laboratory studies were highly correlated with those from the species distributions (r = 0.87). The thermal optima were less strongly correlated (r = 0.69). For most species, we did not detect thermal maxima from their observed distributions so were unable to compare to laboratory-based estimates. The results suggest that laboratory studies have the potential to be highly transportable to predicting lower thermal limits and thermal optima of mosquitoes in the field. At the same time, lab-based models likely capture physiological limits on mosquito persistence at high temperatures that are not apparent from field-based observational studies but may critically determine mosquito responses to climate warming. Our results indicate that lab-based and field-based studies are highly complementary; performing the analyses in concert can help to more comprehensively understand vector response to climate change.
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Affiliation(s)
- Tejas S. Athni
- Harvard Medical School, Boston, Massachusetts, United States of America
- Department of Biology, Stanford University, Stanford, California, United States of America
| | - Marissa L. Childs
- Emmett Interdisciplinary Program in Environment and Resources, Stanford University, Stanford, California, United States of America
- Center for the Environment, Harvard University, Cambridge, Massachusetts, United States of America
| | - Caroline K. Glidden
- Department of Biology, Stanford University, Stanford, California, United States of America
- Stanford Institute for Human-centered Artificial Intelligence, Stanford University, Stanford, California, United States of America
| | - Erin A. Mordecai
- Department of Biology, Stanford University, Stanford, California, United States of America
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Brettell LE, Hoque AF, Joseph TS, Dhokiya V, Hornett EA, Hughes GL, Heinz E. Mosquitoes reared in distinct insectaries within an institution in close spatial proximity possess significantly divergent microbiomes. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2024:2024.08.28.610121. [PMID: 39257775 PMCID: PMC11383675 DOI: 10.1101/2024.08.28.610121] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 09/12/2024]
Abstract
The microbiome affects important aspects of mosquito biology and differences in microbial composition can affect the outcomes of laboratory studies. To determine how the biotic and abiotic conditions in an insectary affect the composition of the bacterial microbiome of mosquitoes we reared mosquitoes from a single cohort of eggs from one genetically homogeneous inbred Aedes aegypti colony, which were split into three batches, and transferred to each of three different insectaries located within the Liverpool School of Tropical Medicine. Using three replicate trays per insectary, we assessed and compared the bacterial microbiome composition as mosquitoes developed from these eggs. We also characterised the microbiome of the mosquitoes' food sources, measured environmental conditions over time in each climate-controlled insectary, and recorded development and survival of mosquitoes. While mosquito development was overall similar between all three insectaries, we saw differences in microbiome composition between mosquitoes from each insectary. Furthermore, bacterial input via food sources, potentially followed by selective pressure of temperature stability and range, did affect the microbiome composition. At both adult and larval stages, specific members of the mosquito microbiome were associated with particular insectaries; and the insectary with less stable and cooler conditions resulted in slower pupation rate and higher diversity of the larval microbiome. Tray and cage effects were also seen in all insectaries, with different bacterial taxa implicated between insectaries. These results highlight the necessity of considering the variability and effects of different microbiome composition even in experiments carried out in a laboratory environment starting with eggs from one batch; and highlights the impact of even minor inconsistencies in rearing conditions due to variation of temperature and humidity.
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Affiliation(s)
- Laura E. Brettell
- Department of Vector biology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK
- School of Science, Engineering and Environment, University of Salford, Manchester, M5 4WT, UK
| | - Ananya F. Hoque
- Department of Vector biology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK
- The Roslin Institute, Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Midlothian, EH25 9RG, UK
| | - Tara S. Joseph
- Department of Vector biology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK
| | - Vishaal Dhokiya
- Department of Vector biology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK
| | - Emily A. Hornett
- Department of Vector biology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK
- Department of Evolution, Ecology and Behaviour, University of Liverpool, Liverpool, L69 7ZB, UK
| | - Grant L. Hughes
- Department of Vector biology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK
- Department of Tropical Disease Biology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK
| | - Eva Heinz
- Department of Vector biology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK
- Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK
- Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, G4 0RE, Glasgow, UK
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27
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Shah N, Irshad M, Murad W, Hamayun M, Qadir M, Hussain A, Begum HA, Alrefaei AF, Almutairi MH, Ahmad A, Ali S. IAA is more effective than EDTA in enhancing phytoremediation potential for cadmium and copper contaminated soils. BMC PLANT BIOLOGY 2024; 24:815. [PMID: 39210254 PMCID: PMC11360555 DOI: 10.1186/s12870-024-05329-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 04/22/2024] [Accepted: 06/24/2024] [Indexed: 09/04/2024]
Abstract
Enhanced phytoremediation offers a rapid and eco-friendly approach for cleaning agricultural soil contaminated with copper and cadmium which pose a direct threat to food scarcity and security. The current study aimed to compare the effectiveness of the two commonly used additives, IAA and EDTA, for the remediation of copper (Cu) and cadmium (Cd) contaminated soils using sunflower and maize. The plants were cultivated in pots under controlled conditions with four sets of treatments: control (0), Cu50/Cd50, Cu50/Cd50 + EDTA, and Cu50/Cd50 + IAA. The results showed that Cu50/Cd50 mg/kg drastically compromised the phytoremediation potential of both plants, as evident by reduced shoot and root length, and lower biomass. However, the augmentation of Cu50/Cd50 with EDTA or IAA improved the tested parameters. In sunflower, EDTA enhanced the accumulation of Cu and Cd by 58% and 21%, respectively, and improved plant biomass by 41%, compared to control treatment. However, IAA exhibited higher accumulation of Cu and Cd by 64% and 25%, respectively, and enhanced plant biomass by 43%. In case of maize, IAA was superior to EDTA which enhanced the accumulation of Cu and Cd by 87% and 32% respectively, and increased the plant biomass by 57%, compared to control treatment. Our findings demonstrate that foliar IAA is more effective than EDTA in enhancing the phytoremediation potential of sunflower and maize for Cu and Cd.
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Affiliation(s)
- Naila Shah
- Department of Botany, Garden Campus, Abdul Wali Khan University Mardan, Mardan, Pakistan
- Department of Botany, Government Girls Degree College, Lundkhwar, Mardan, Pakistan
| | - Muhammad Irshad
- Department of Botany, Garden Campus, Abdul Wali Khan University Mardan, Mardan, Pakistan.
| | - Waheed Murad
- Department of Botany, Garden Campus, Abdul Wali Khan University Mardan, Mardan, Pakistan
| | - Muhammad Hamayun
- Department of Botany, Garden Campus, Abdul Wali Khan University Mardan, Mardan, Pakistan
| | - Muhammad Qadir
- Department of Botany, Garden Campus, Abdul Wali Khan University Mardan, Mardan, Pakistan
| | - Anwar Hussain
- Department of Botany, Garden Campus, Abdul Wali Khan University Mardan, Mardan, Pakistan
| | - Hussan Ara Begum
- Department of Botany, Garden Campus, Abdul Wali Khan University Mardan, Mardan, Pakistan
| | | | - Mikhlid H Almutairi
- Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia
| | - Ayaz Ahmad
- Department of Biotechnology, Garden Campus, Abdul Wali Khan University Mardan, Mardan, Pakistan
| | - Sajid Ali
- Department of Horticulture and Life Science, Yeungnam University, Gyeongsan, Republic of Korea.
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28
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de Souza WM, Weaver SC. Effects of climate change and human activities on vector-borne diseases. Nat Rev Microbiol 2024; 22:476-491. [PMID: 38486116 DOI: 10.1038/s41579-024-01026-0] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 02/13/2024] [Indexed: 03/18/2024]
Abstract
Vector-borne diseases are transmitted by haematophagous arthropods (for example, mosquitoes, ticks and sandflies) to humans and wild and domestic animals, with the largest burden on global public health disproportionately affecting people in tropical and subtropical areas. Because vectors are ectothermic, climate and weather alterations (for example, temperature, rainfall and humidity) can affect their reproduction, survival, geographic distribution and, consequently, ability to transmit pathogens. However, the effects of climate change on vector-borne diseases can be multifaceted and complex, sometimes with ambiguous consequences. In this Review, we discuss the potential effects of climate change, weather and other anthropogenic factors, including land use, human mobility and behaviour, as possible contributors to the redistribution of vectors and spread of vector-borne diseases worldwide.
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Affiliation(s)
- William M de Souza
- Department of Microbiology, Immunology and Molecular Genetics, University of Kentucky, College of Medicine, Lexington, KY, USA
- World Reference Center for Emerging Viruses and Arboviruses, University of Texas Medical Branch, Galveston, TX, USA
- Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, TX, USA
- Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, USA
- Global Virus Network, Baltimore, MD, USA
| | - Scott C Weaver
- World Reference Center for Emerging Viruses and Arboviruses, University of Texas Medical Branch, Galveston, TX, USA.
- Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, TX, USA.
- Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, USA.
- Global Virus Network, Baltimore, MD, USA.
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29
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Pruszynski CA, Buckner EA, Burkett-Cadena ND, Hugo LE, Leal AL, Caragata EP. Estimation of population age structure, daily survival rates, and potential to support dengue virus transmission for Florida Keys Aedes aegypti via transcriptional profiling. PLoS Negl Trop Dis 2024; 18:e0012350. [PMID: 39137188 PMCID: PMC11321583 DOI: 10.1371/journal.pntd.0012350] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/15/2024] [Accepted: 07/08/2024] [Indexed: 08/15/2024] Open
Abstract
Aedes aegypti is an important vector of dengue virus and other arboviruses that affect human health. After being ingested in an infectious bloodmeal, but before being transmitted from mosquito to human, dengue virus must disseminate from the vector midgut into the hemocoel and then the salivary glands. This process, the extrinsic incubation period, typically takes 6-14 days. Since older mosquitoes are responsible for transmission, understanding the age structure of vector populations is important. Transcriptional profiling can facilitate predictions of the age structures of mosquito populations, critical for estimating their potential for pathogen transmission. In this study, we utilized a two-gene transcript model to assess the age structure and daily survival rates of three populations (Key West, Marathon, and Key Largo) of Ae. aegypti from the Florida Keys, United States, where repeated outbreaks of autochthonous dengue transmission have recently occurred. We found that Key Largo had the youngest Ae. aegypti population with the lowest daily survival rate, while Key West had the oldest population and highest survival rate. Across sites, 22.67% of Ae. aegypti females were likely old enough to transmit dengue virus (at least 15 days post emergence). Computed estimates of the daily survival rate (0.8364 using loglinear and 0.8660 using non-linear regression), indicate that dengue vectors in the region experienced relatively low daily mortality. Collectively, our data suggest that Ae. aegypti populations across the Florida Keys harbor large numbers of older individuals, which likely contributes to the high risk of dengue transmission in the area.
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Affiliation(s)
- Catherine A. Pruszynski
- Florida Keys Mosquito Control District, Marathon, Florida, United States of America
- University of Florida, Institute of Food and Agricultural Sciences, Department of Entomology and Nematology, Florida Medical Entomology Laboratory, Vero Beach, Florida, United States of America
| | - Eva A. Buckner
- University of Florida, Institute of Food and Agricultural Sciences, Department of Entomology and Nematology, Florida Medical Entomology Laboratory, Vero Beach, Florida, United States of America
| | - Nathan D. Burkett-Cadena
- University of Florida, Institute of Food and Agricultural Sciences, Department of Entomology and Nematology, Florida Medical Entomology Laboratory, Vero Beach, Florida, United States of America
| | - Leon E. Hugo
- Mosquito Control Laboratory, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia
| | - Andrea L. Leal
- Florida Keys Mosquito Control District, Marathon, Florida, United States of America
| | - Eric P. Caragata
- University of Florida, Institute of Food and Agricultural Sciences, Department of Entomology and Nematology, Florida Medical Entomology Laboratory, Vero Beach, Florida, United States of America
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30
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Cruz EI, Salazar FV, Aguila AMA, Villaruel-Jagmis MV, Ramos J, Paul RE. Current and lagged associations of meteorological variables and Aedes mosquito indices with dengue incidence in the Philippines. PLoS Negl Trop Dis 2024; 18:e0011603. [PMID: 39042669 PMCID: PMC11296630 DOI: 10.1371/journal.pntd.0011603] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/21/2023] [Revised: 08/02/2024] [Accepted: 06/27/2024] [Indexed: 07/25/2024] Open
Abstract
BACKGROUND Dengue is an increasing health burden that has spread throughout the tropics and sub-tropics. There is currently no effective vaccine and control is only possible through integrated vector management. Early warning systems (EWS) to alert potential dengue outbreaks are currently being explored but despite showing promise are yet to come to fruition. This study addresses the association of meteorological variables with both mosquito indices and dengue incidences and assesses the added value of additionally using mosquito indices for predicting dengue incidences. METHODOLOGY/PRINCIPAL FINDINGS Entomological surveys were carried out monthly for 14 months in six sites spread across three environmentally different cities of the Philippines. Meteorological and dengue data were acquired. Non-linear generalized additive models were fitted to test associations of the meteorological variables with both mosquito indices and dengue cases. Rain and the diurnal temperature range (DTR) contributed most to explaining the variation in both mosquito indices and number of dengue cases. DTR and minimum temperature also explained variation in dengue cases occurring one and two months later and may offer potentially useful variables for an EWS. The number of adult mosquitoes did associate with the number of dengue cases, but contributed no additional value to meteorological variables for explaining variation in dengue cases. CONCLUSIONS/SIGNIFICANCE The use of meteorological variables to predict future risk of dengue holds promise. The lack of added value of using mosquito indices confirms several previous studies and given the onerous nature of obtaining such information, more effort should be placed on improving meteorological information at a finer scale to evaluate efficacy in early warning of dengue outbreaks.
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Affiliation(s)
- Estrella I. Cruz
- Department of Medical Entomology, Research Institute for Tropical Medicine, Filinvest Corporate City, Alabang, Muntinlupa City, Philippines
| | - Ferdinand V. Salazar
- Department of Medical Entomology, Research Institute for Tropical Medicine, Filinvest Corporate City, Alabang, Muntinlupa City, Philippines
| | - Ariza Minelle A. Aguila
- Department of Medical Entomology, Research Institute for Tropical Medicine, Filinvest Corporate City, Alabang, Muntinlupa City, Philippines
| | - Mary Vinessa Villaruel-Jagmis
- Department of Medical Entomology, Research Institute for Tropical Medicine, Filinvest Corporate City, Alabang, Muntinlupa City, Philippines
| | - Jennifer Ramos
- Department of Medical Entomology, Research Institute for Tropical Medicine, Filinvest Corporate City, Alabang, Muntinlupa City, Philippines
| | - Richard E. Paul
- Ecology and Emergence of Arthropod-borne Pathogens unit, Institut Pasteur, Université Paris-Cité, Centre National de Recherche Scientifique (CNRS) UMR 2000, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) USC 1510, Paris, France
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31
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Fay RL, Cruz-Loya M, Keyel AC, Price DC, Zink SD, Mordecai EA, Ciota AT. Population-specific thermal responses contribute to regional variability in arbovirus transmission with changing climates. iScience 2024; 27:109934. [PMID: 38799579 PMCID: PMC11126822 DOI: 10.1016/j.isci.2024.109934] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/26/2023] [Revised: 12/05/2023] [Accepted: 05/05/2024] [Indexed: 05/29/2024] Open
Abstract
Temperature is increasing globally, and vector-borne diseases are particularly responsive to such increases. While it is known that temperature influences mosquito life history traits, transmission models have not historically considered population-specific effects of temperature. We assessed the interaction between Culex pipiens population and temperature in New York State (NYS) and utilized novel empirical data to inform predictive models of West Nile virus (WNV) transmission. Genetically and regionally distinct populations from NYS were reared at various temperatures, and life history traits were monitored and used to inform trait-based models. Variation in Cx. pipiens life history traits and population-dependent thermal responses account for a predicted 2.9°C difference in peak transmission that is reflected in regional differences in WNV prevalence. We additionally identified genetic signatures that may contribute to distinct thermal responses. Together, these data demonstrate how population variation contributes to significant geographic variability in arbovirus transmission with changing climates.
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Affiliation(s)
- Rachel L. Fay
- Department of Biomedical Sciences, State University of New York at Albany School of Public Health, Rensselaer, NY, USA
- The Arbovirus Laboratory, Wadsworth Center, New York State Department of Health, Slingerlands, NY, USA
| | | | - Alexander C. Keyel
- The Arbovirus Laboratory, Wadsworth Center, New York State Department of Health, Slingerlands, NY, USA
| | - Dana C. Price
- Department of Entomology, Rutgers University, New Brunswick, NJ, USA
| | - Steve D. Zink
- The Arbovirus Laboratory, Wadsworth Center, New York State Department of Health, Slingerlands, NY, USA
| | | | - Alexander T. Ciota
- Department of Biomedical Sciences, State University of New York at Albany School of Public Health, Rensselaer, NY, USA
- The Arbovirus Laboratory, Wadsworth Center, New York State Department of Health, Slingerlands, NY, USA
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32
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Kawiecki AB, Morrison AC, Barker CM. Spatial and temporal analysis on the impact of ultra-low volume indoor insecticide spraying on Aedes aegypti household density. Parasit Vectors 2024; 17:254. [PMID: 38863023 PMCID: PMC11165869 DOI: 10.1186/s13071-024-06308-3] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/10/2024] [Accepted: 04/25/2024] [Indexed: 06/13/2024] Open
Abstract
BACKGROUND Aedes aegypti is the primary mosquito vector for several arboviruses, such as dengue, chikungunya and Zika viruses, which cause frequent outbreaks of human disease in tropical and subtropical regions. Control of these outbreaks relies on vector control, commonly in the form of insecticide sprays that target adult female mosquitoes. However, the spatial coverage and frequency of sprays needed to optimize effectiveness are unclear. In this study, we characterize the effect of ultra-low-volume (ULV) indoor spraying of pyrethroid insecticides on Ae. aegypti abundance within households. We also evaluate the effects of spray events during recent time periods or in neighboring households. Improved understanding of the duration and distance of the impact of a spray intervention on Ae. aegypti populations can inform vector control interventions, in addition to modeling efforts that contrast vector control strategies. METHODS This project analyzes data from two large-scale experiments that involved six cycles of indoor pyrethroid spray applications in 2 years in the Amazonian city of Iquitos, Peru. We developed spatial multi-level models to disentangle the reduction in Ae. aegypti abundance that resulted from (i) recent ULV treatment within households and (ii) ULV treatment of adjacent or nearby households. We compared fits of models across a range of candidate weighting schemes for the spray effect, based on different temporal and spatial decay functions to understand lagged ULV effects. RESULTS Our results suggested that the reduction of Ae. aegypti in a household was mainly due to spray events occurring within the same household, with no additional effect of sprays that occurred in neighboring households. Effectiveness of a spray intervention should be measured based on time since the most recent spray event, as we found no cumulative effect of sequential sprays. Based on our model, we estimated the spray effect is reduced by 50% approximately 28 days after the spray event. CONCLUSIONS The reduction of Ae. aegypti in a household was mainly determined by the number of days since the last spray intervention in that same household, highlighting the importance of spray coverage in high-risk areas with a spray frequency determined by local viral transmission dynamics.
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Affiliation(s)
| | | | - Christopher M Barker
- University of California Davis, Davis, CA, USA.
- Pacific Southwest Center of Excellence in Vector-Borne Diseases, University of California Davis, Davis, CA, USA.
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33
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Aslan IH, Pourtois JD, Chamberlin AJ, Mitchell KR, Mari L, Lwiza KM, Wood CL, Mordecai EA, Yu A, Tuan R, Palasio RGS, Monteiro AMV, Kirk D, Athni TS, Sokolow SH, N’Goran EK, Diakite NR, Ouattara M, Gatto M, Casagrandi R, Little DC, Ozretich RW, Norman R, Allan F, Brierley AS, Liu P, Pereira TA, De Leo GA. Re-assessing thermal response of schistosomiasis transmission risk: Evidence for a higher thermal optimum than previously predicted. PLoS Negl Trop Dis 2024; 18:e0011836. [PMID: 38857289 PMCID: PMC11207148 DOI: 10.1371/journal.pntd.0011836] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/30/2023] [Revised: 06/26/2024] [Accepted: 05/23/2024] [Indexed: 06/12/2024] Open
Abstract
The geographical range of schistosomiasis is affected by the ecology of schistosome parasites and their obligate host snails, including their response to temperature. Previous models predicted schistosomiasis' thermal optimum at 21.7°C, which is not compatible with the temperature in sub-Saharan Africa (SSA) regions where schistosomiasis is hyperendemic. We performed an extensive literature search for empirical data on the effect of temperature on physiological and epidemiological parameters regulating the free-living stages of S. mansoni and S. haematobium and their obligate host snails, i.e., Biomphalaria spp. and Bulinus spp., respectively. We derived nonlinear thermal responses fitted on these data to parameterize a mechanistic, process-based model of schistosomiasis. We then re-cast the basic reproduction number and the prevalence of schistosome infection as functions of temperature. We found that the thermal optima for transmission of S. mansoni and S. haematobium range between 23.1-27.3°C and 23.6-27.9°C (95% CI) respectively. We also found that the thermal optimum shifts toward higher temperatures as the human water contact rate increases with temperature. Our findings align with an extensive dataset of schistosomiasis prevalence in SSA. The refined nonlinear thermal-response model developed here suggests a more suitable current climate and a greater risk of increased transmission with future warming for more than half of the schistosomiasis suitable regions with mean annual temperature below the thermal optimum.
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Affiliation(s)
- Ibrahim Halil Aslan
- Department of Biology, Stanford University, Stanford, California, United States of America
- Hopkins Marine Station, Stanford University, Pacific Grove, California, United States of America
| | - Julie D. Pourtois
- Department of Biology, Stanford University, Stanford, California, United States of America
- Hopkins Marine Station, Stanford University, Pacific Grove, California, United States of America
| | - Andrew J. Chamberlin
- Hopkins Marine Station, Stanford University, Pacific Grove, California, United States of America
| | - Kaitlyn R. Mitchell
- Department of Biology, Stanford University, Stanford, California, United States of America
- Hopkins Marine Station, Stanford University, Pacific Grove, California, United States of America
| | - Lorenzo Mari
- Department of Electronics, Information and Bioengineering, Politecnico di Milano, Milano, Italy
| | - Kamazima M. Lwiza
- School of Marine and Atmospheric Sciences, Stony Brook University, New York, New York, United States of America
| | - Chelsea L. Wood
- School of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington, United States of America
| | - Erin A. Mordecai
- Department of Biology, Stanford University, Stanford, California, United States of America
- Woods Institute for the Environment, Stanford University, Stanford, California, United States of America
| | - Ao Yu
- Department of Earth System Science, Stanford University, Stanford, California, United States of America
| | - Roseli Tuan
- Pasteur Institute, São Paulo Health Public Office, São Paulo, Brazil
| | | | | | - Devin Kirk
- Department of Biology, Stanford University, Stanford, California, United States of America
| | - Tejas S. Athni
- Department of Biology, Stanford University, Stanford, California, United States of America
- Harvard Medical School, Boston, Massachusetts, United States of America
| | - Susanne H. Sokolow
- Department of Biology, Stanford University, Stanford, California, United States of America
- Woods Institute for the Environment, Stanford University, Stanford, California, United States of America
| | | | | | | | - Marino Gatto
- Department of Electronics, Information and Bioengineering, Politecnico di Milano, Milano, Italy
| | - Renato Casagrandi
- Department of Electronics, Information and Bioengineering, Politecnico di Milano, Milano, Italy
| | - David C. Little
- Institute of Aquaculture, University of Stirling, Stirling, United Kingdom
| | - Reed W. Ozretich
- Institute of Aquaculture, University of Stirling, Stirling, United Kingdom
| | - Rachel Norman
- Computing Science and Mathematics, University of Stirling, Stirling, United Kingdom
| | - Fiona Allan
- Department of Life Sciences, Natural History Museum, London, United Kingdom
| | - Andrew S. Brierley
- Scottish Oceans Institute, School of Biology, University of St. Andrews, St. Andrews, United Kingdom
| | - Ping Liu
- School of Marine and Atmospheric Sciences, Stony Brook University, New York, New York, United States of America
| | - Thiago A. Pereira
- Institute for Stem Cell Biology and Regenerative Medicine, School of Medicine, Stanford University, Stanford, California, United States of America
| | - Giulio A. De Leo
- Department of Biology, Stanford University, Stanford, California, United States of America
- Hopkins Marine Station, Stanford University, Pacific Grove, California, United States of America
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34
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Aslan IH, Pourtois JD, Chamberlin AJ, Mitchell KR, Mari L, Lwiza KM, Wood CL, Mordecai EA, Yu A, Tuan R, Palasio RGS, Monteiro AM, Kirk D, Athni TS, Sokolow SH, N’Goran EK, Diakite NR, Ouattara M, Gatto M, Casagrandi R, Little DC, Ozretich RW, Norman R, Allan F, Brierley AS, Liu P, Pereira TA, De Leo GA. Re-assessing thermal response of schistosomiasis transmission risk: evidence for a higher thermal optimum than previously predicted. MEDRXIV : THE PREPRINT SERVER FOR HEALTH SCIENCES 2024:2024.01.04.24300851. [PMID: 38826336 PMCID: PMC11142288 DOI: 10.1101/2024.01.04.24300851] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/04/2024]
Abstract
The geographical range of schistosomiasis is affected by the ecology of schistosome parasites and their obligate host snails, including their response to temperature. Previous models predicted schistosomiasis' thermal optimum at 21.7 °C, which is not compatible with the temperature in sub-Saharan Africa (SSA) regions where schistosomiasis is hyperendemic. We performed an extensive literature search for empirical data on the effect of temperature on physiological and epidemiological parameters regulating the free-living stages of S. mansoni and S. haematobium and their obligate host snails, i.e., Biomphalaria spp. and Bulinus spp., respectively. We derived nonlinear thermal responses fitted on these data to parameterize a mechanistic, process-based model of schistosomiasis. We then re-cast the basic reproduction number and the prevalence of schistosome infection as functions of temperature. We found that the thermal optima for transmission of S. mansoni and S. haematobium range between 23.1-27.3 °C and 23.6-27.9 °C (95 % CI) respectively. We also found that the thermal optimum shifts toward higher temperatures as the human water contact rate increases with temperature. Our findings align with an extensive dataset of schistosomiasis prevalence in SSA. The refined nonlinear thermal-response model developed here suggests a more suitable current climate and a greater risk of increased transmission with future warming for more than half of the schistosomiasis suitable regions with mean annual temperature below the thermal optimum.
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Affiliation(s)
- Ibrahim Halil Aslan
- Department of Biology, Stanford University, Stanford, CA, USA
- Hopkins Marine Station, Stanford University, Pacific Grove, CA, USA
| | - Julie D. Pourtois
- Department of Biology, Stanford University, Stanford, CA, USA
- Hopkins Marine Station, Stanford University, Pacific Grove, CA, USA
| | | | - Kaitlyn R. Mitchell
- Department of Biology, Stanford University, Stanford, CA, USA
- Hopkins Marine Station, Stanford University, Pacific Grove, CA, USA
| | - Lorenzo Mari
- Department of Electronics, Information and Bioengineering, Politecnico di Milano, Milano, Italy
| | - Kamazima M. Lwiza
- School of Marine and Atmospheric Sciences Stony Brook University, New York, NY, USA
| | - Chelsea L. Wood
- School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, USA
| | - Erin A. Mordecai
- Department of Biology, Stanford University, Stanford, CA, USA
- Woods Institute for the Environment, Stanford University, Stanford, CA, USA
| | - Ao Yu
- Department of Earth System Science, Stanford University, Stanford, CA, USA
| | - Roseli Tuan
- Pasteur Institute, São Paulo Health Public Office, São Paulo, SP, Brazil
| | | | | | - Devin Kirk
- Department of Biology, Stanford University, Stanford, CA, USA
| | - Tejas S. Athni
- Department of Biology, Stanford University, Stanford, CA, USA
- Harvard Medical School, Boston, MA, USA
| | - Susanne H. Sokolow
- Department of Biology, Stanford University, Stanford, CA, USA
- Woods Institute for the Environment, Stanford University, Stanford, CA, USA
| | | | - Nana R. Diakite
- Université Félix Houphouët-Boigny, 22 BP 770, Abidjan 22, Côte d’Ivoire
| | - Mamadou Ouattara
- Université Félix Houphouët-Boigny, 22 BP 770, Abidjan 22, Côte d’Ivoire
| | - Marino Gatto
- Department of Electronics, Information and Bioengineering, Politecnico di Milano, Milano, Italy
| | - Renato Casagrandi
- Department of Electronics, Information and Bioengineering, Politecnico di Milano, Milano, Italy
| | - David C. Little
- Institute of Aquaculture, University of Stirling, Stirling, UK
| | | | - Rachel Norman
- Computing Science and Mathematics, University of Stirling, Stirling, UK
| | - Fiona Allan
- Department of Life Sciences, Natural History Museum, London, UK
| | - Andrew S. Brierley
- Scottish Oceans Institute, School of Biology, University of St. Andrews, St. Andrews, UK
| | - Ping Liu
- School of Marine and Atmospheric Sciences Stony Brook University, New York, NY, USA
| | - Thiago A. Pereira
- Institute for Stem Cell Biology and Regenerative Medicine, School of Medicine, Stanford University, Stanford, CA, USA
| | - Giulio A. De Leo
- Department of Biology, Stanford University, Stanford, CA, USA
- Hopkins Marine Station, Stanford University, Pacific Grove, CA, USA
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35
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Zhang X, Li J, Gerry AC. Seasonal change and influence of environmental variables on host-seeking activity of the biting midge Culicoides sonorensis at a southern California dairy, USA. Parasit Vectors 2024; 17:212. [PMID: 38730488 PMCID: PMC11083819 DOI: 10.1186/s13071-024-06290-w] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/25/2024] [Accepted: 04/19/2024] [Indexed: 05/13/2024] Open
Abstract
BACKGROUND As a primary vector of bluetongue virus (BTV) in the US, seasonal abundance and diel flight activity of Culicoides sonorensis has been documented, but few studies have examined how time of host-seeking activity is impacted by environmental factors. This knowledge is essential for interpreting surveillance data and modeling pathogen transmission risk. METHODS The diel host-seeking activity of C. sonorensis was studied on a California dairy over 3 years using a time-segregated trap baited with CO2. The relationship between environmental variables and diel host-seeking activity (start, peak, and duration of activity) of C. sonorensis was evaluated using multiple linear regression. Fisher's exact test and paired-sample z-test were used to evaluate the seasonal difference and parity difference on diel host-seeking activity. RESULTS Host-seeking by C. sonorensis began and reached an activity peak before sunset at a higher frequency during colder months relative to warmer months. The time that host-seeking activity occurred was associated low and high daily temperature as well as wind speed at sunset. Colder temperatures and a greater diurnal temperature range were associated with an earlier peak in host-seeking. Higher wind speeds at sunset were associated with a delayed peak in host-seeking and a shortened duration of host-seeking. Parous midges reached peak host-seeking activity slightly later than nulliparous midges, possibly because of the need for oviposition by gravid females before returning to host-seeking. CONCLUSIONS This study demonstrates that during colder months C. sonorensis initiates host-seeking and reaches peak host-seeking activity earlier relative to sunset, often even before sunset, compared to warmer months. Therefore, the commonly used UV light-baited traps are ineffective for midge surveillance before sunset. Based on this study, surveillance methods that do not rely on light trapping would provide a more accurate estimate of host-biting risk across seasons. The association of environmental factors to host-seeking shown in this study can be used to improve modeling or prediction of host-seeking activity. This study identified diurnal temperature range as associated with host-seeking activity, suggesting that Culicoides may respond to a rapidly decreasing temperature by shifting to an earlier host-seeking time, though this association needs further study.
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Affiliation(s)
- Xinmi Zhang
- Department of Entomology, University of California Riverside, Riverside, CA, USA.
| | - Jun Li
- Department of Statistics, University of California Riverside, Riverside, CA, USA
| | - Alec C Gerry
- Department of Entomology, University of California Riverside, Riverside, CA, USA.
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Trzebny A, Nahimova O, Dabert M. High temperatures and low humidity promote the occurrence of microsporidians (Microsporidia) in mosquitoes (Culicidae). Parasit Vectors 2024; 17:187. [PMID: 38605410 PMCID: PMC11008030 DOI: 10.1186/s13071-024-06254-0] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/26/2023] [Accepted: 03/20/2024] [Indexed: 04/13/2024] Open
Abstract
BACKGROUND In the context of climate change, a growing concern is that vector-pathogen or host-parasite interactions may be correlated with climatic factors, especially increasing temperatures. In the present study, we used a mosquito-microsporidian model to determine the impact of environmental factors such as temperature, humidity, wind and rainfall on the occurrence rates of opportunistic obligate microparasites (Microsporidia) in hosts from a family that includes important disease vectors (Culicidae). METHODS In our study, 3000 adult mosquitoes collected from the field over 3 years were analysed. Mosquitoes and microsporidia were identified using PCR and sequencing of the hypervariable V5 region of the small subunit ribosomal RNA gene and a shortened fragment of the cytochrome c oxidase subunit I gene, respectively. RESULTS DNA metabarcoding was used to identify nine mosquito species, all of which were hosts of 12 microsporidian species. The prevalence of microsporidian DNA across all mosquito samples was 34.6%. Microsporidian prevalence in mosquitoes was more frequent during warm months (> 19 °C; humidity < 65%), as was the co-occurrence of two or three microsporidian species in a single host individual. During warm months, microsporidian occurrence was noted 1.6-fold more often than during the cold periods. Among the microsporidians found in the mosquitoes, five (representing the genera Enterocytospora, Vairimorpha and Microsporidium) were positively correlated with an increase in temperature, whereas one (Hazardia sp.) was significantly correlated with a decrease in temperature. Threefold more microsporidian co-occurrences were recorded in the warm months than in the cold months. CONCLUSIONS These results suggest that the susceptibility of mosquitoes to parasite occurrence is primarily determined by environmental conditions, such as, for example, temperatures > 19 °C and humidity not exceeding 62%. Collectively, our data provide a better understanding of the effects of the environment on microsporidian-mosquito interactions.
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Affiliation(s)
- Artur Trzebny
- Molecular Biology Techniques Laboratory, Faculty of Biology, Adam Mickiewicz University, Poznan, Poland.
| | - Olena Nahimova
- Molecular Biology Techniques Laboratory, Faculty of Biology, Adam Mickiewicz University, Poznan, Poland
- Genetics and Cytology Department, School of Biology, V.N. Karazin Kharkiv National University, Kharkiv, Ukraine
| | - Miroslawa Dabert
- Molecular Biology Techniques Laboratory, Faculty of Biology, Adam Mickiewicz University, Poznan, Poland
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Johnson RM, Stopard IJ, Byrne HM, Armstrong PM, Brackney DE, Lambert B. Investigating the dose-dependency of the midgut escape barrier using a mechanistic model of within-mosquito dengue virus population dynamics. PLoS Pathog 2024; 20:e1011975. [PMID: 38557892 PMCID: PMC11008821 DOI: 10.1371/journal.ppat.1011975] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/28/2023] [Revised: 04/11/2024] [Accepted: 01/16/2024] [Indexed: 04/04/2024] Open
Abstract
Arboviruses can emerge rapidly and cause explosive epidemics of severe disease. Some of the most epidemiologically important arboviruses, including dengue virus (DENV), Zika virus (ZIKV), Chikungunya (CHIKV) and yellow fever virus (YFV), are transmitted by Aedes mosquitoes, most notably Aedes aegypti and Aedes albopictus. After a mosquito blood feeds on an infected host, virus enters the midgut and infects the midgut epithelium. The virus must then overcome a series of barriers before reaching the mosquito saliva and being transmitted to a new host. The virus must escape from the midgut (known as the midgut escape barrier; MEB), which is thought to be mediated by transient changes in the permeability of the midgut-surrounding basal lamina layer (BL) following blood feeding. Here, we present a mathematical model of the within-mosquito population dynamics of DENV (as a model system for mosquito-borne viruses more generally) that includes the interaction of the midgut and BL which can account for the MEB. Our results indicate a dose-dependency of midgut establishment of infection as well as rate of escape from the midgut: collectively, these suggest that the extrinsic incubation period (EIP)-the time taken for DENV virus to be transmissible after infection-is shortened when mosquitoes imbibe more virus. Additionally, our experimental data indicate that multiple blood feeding events, which more closely mimic mosquito-feeding behavior in the wild, can hasten the course of infections, and our model predicts that this effect is sensitive to the amount of virus imbibed. Our model indicates that mutations to the virus which impact its replication rate in the midgut could lead to even shorter EIPs when double-feeding occurs. Mechanistic models of within-vector viral infection dynamics provide a quantitative understanding of infection dynamics and could be used to evaluate novel interventions that target the mosquito stages of the infection.
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Affiliation(s)
- Rebecca M. Johnson
- Center for Vector-Borne and Zoonotic Diseases, Department of Entomology, The Connecticut Agricultural Experiment Station, New Haven, Connecticut, United States of America
| | - Isaac J. Stopard
- MRC Centre for Global Infectious Disease Analysis, School of Public Health, Faculty of Medicine, Imperial College London, London, United Kingdom
| | - Helen M. Byrne
- Mathematical Institute, University of Oxford, Oxford, United Kingdom
| | - Philip M. Armstrong
- Center for Vector-Borne and Zoonotic Diseases, Department of Entomology, The Connecticut Agricultural Experiment Station, New Haven, Connecticut, United States of America
| | - Douglas E. Brackney
- Center for Vector-Borne and Zoonotic Diseases, Department of Entomology, The Connecticut Agricultural Experiment Station, New Haven, Connecticut, United States of America
| | - Ben Lambert
- Department of Statistics, University of Oxford, Oxford, United Kingdom
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Hug DOH, Kropf A, Amann MO, Koella JC, Verhulst NO. Unexpected behavioural adaptation of yellow fever mosquitoes in response to high temperatures. Sci Rep 2024; 14:3659. [PMID: 38351076 PMCID: PMC10864274 DOI: 10.1038/s41598-024-54374-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/07/2023] [Accepted: 02/12/2024] [Indexed: 02/16/2024] Open
Abstract
Temperature is a major ecological driver of mosquito-borne diseases as it influences the life-history of both the mosquito and the pathogen harboured within it. Understanding the mosquitoes' thermal biology is essential to inform risk prediction models of such diseases. Mosquitoes can respond to temperatures by microhabitat selection through thermal preference. However, it has not yet been considered that mosquitoes are likely to adapt to changing temperatures, for example during climate change, and alter their preference over evolutionary time. We investigated this by rearing six cohorts of the yellow fever mosquito Aedes aegypti at two temperatures (24 °C, 30 °C) for 20 generations and used these cohorts to explicitly separate the effects of long-term evolution and within-generation acclimation on their thermal preferences in a thermal gradient of 20-35 °C. We found that warm-evolved mosquitoes spent 31.5% less time at high temperatures, which affects their efficiency as a vector. This study reveals the complex interplay of experimental evolution, rearing temperatures, and thermal preference in Ae. aegypti mosquitoes. It highlights the significance of incorporating mosquito microhabitat selection in disease transmission models, especially in the context of climate change.
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Affiliation(s)
- David O H Hug
- National Centre for Vector Entomology, Institute of Parasitology, Vetsuisse and Medical Faculty, University of Zürich, Zurich, Switzerland
| | - Alida Kropf
- Laboratory of Ecology and Epidemiology of Parasites, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
| | - Marine O Amann
- Laboratory of Ecology and Epidemiology of Parasites, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
| | - Jacob C Koella
- Laboratory of Ecology and Epidemiology of Parasites, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
| | - Niels O Verhulst
- National Centre for Vector Entomology, Institute of Parasitology, Vetsuisse and Medical Faculty, University of Zürich, Zurich, Switzerland.
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Erazo D, Grant L, Ghisbain G, Marini G, Colón-González FJ, Wint W, Rizzoli A, Van Bortel W, Vogels CBF, Grubaugh ND, Mengel M, Frieler K, Thiery W, Dellicour S. Contribution of climate change to the spatial expansion of West Nile virus in Europe. Nat Commun 2024; 15:1196. [PMID: 38331945 PMCID: PMC10853512 DOI: 10.1038/s41467-024-45290-3] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/27/2023] [Accepted: 01/18/2024] [Indexed: 02/10/2024] Open
Abstract
West Nile virus (WNV) is an emerging mosquito-borne pathogen in Europe where it represents a new public health threat. While climate change has been cited as a potential driver of its spatial expansion on the continent, a formal evaluation of this causal relationship is lacking. Here, we investigate the extent to which WNV spatial expansion in Europe can be attributed to climate change while accounting for other direct human influences such as land-use and human population changes. To this end, we trained ecological niche models to predict the risk of local WNV circulation leading to human cases to then unravel the isolated effect of climate change by comparing factual simulations to a counterfactual based on the same environmental changes but a counterfactual climate where long-term trends have been removed. Our findings demonstrate a notable increase in the area ecologically suitable for WNV circulation during the period 1901-2019, whereas this area remains largely unchanged in a no-climate-change counterfactual. We show that the drastic increase in the human population at risk of exposure is partly due to historical changes in population density, but that climate change has also been a critical driver behind the heightened risk of WNV circulation in Europe.
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Affiliation(s)
- Diana Erazo
- Spatial Epidemiology Lab (SpELL), Université Libre de Bruxelles, Brussels, Belgium.
| | - Luke Grant
- Department of Water and Climate, Vrije Universiteit Brussel, Brussels, Belgium
| | - Guillaume Ghisbain
- Spatial Epidemiology Lab (SpELL), Université Libre de Bruxelles, Brussels, Belgium
- Laboratory of Zoology, Research Institute for Biosciences, University of Mons, Mons, Belgium
| | - Giovanni Marini
- Research and Innovation Centre, Fondazione Edmund Mach, San Michele all'Adige, Trento, Italy
| | | | - William Wint
- Environmental Research Group Oxford Ltd, Department of Biology, Mansfield Road, Oxford, OX1 3SZ, UK
| | - Annapaola Rizzoli
- Research and Innovation Centre, Fondazione Edmund Mach, San Michele all'Adige, Trento, Italy
| | - Wim Van Bortel
- Unit Entomology, Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium
- Outbreak Research team, Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium
| | - Chantal B F Vogels
- Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA
| | - Nathan D Grubaugh
- Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA
- Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA
| | - Matthias Mengel
- Department Transformation Pathways, Potsdam Institute for Climate Impact Research (PIK), Potsdam, Germany
| | - Katja Frieler
- Department Transformation Pathways, Potsdam Institute for Climate Impact Research (PIK), Potsdam, Germany
| | - Wim Thiery
- Department of Water and Climate, Vrije Universiteit Brussel, Brussels, Belgium
| | - Simon Dellicour
- Spatial Epidemiology Lab (SpELL), Université Libre de Bruxelles, Brussels, Belgium.
- Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory for Clinical and Epidemiological Virology, KU Leuven, Leuven, Belgium.
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Jaramillo-Ramirez GI, Tacugue MC, Power GM, Qureshi R, Seelig F, Quintero J, Logan JG, Jones RT. A Qualitative Analysis of the Perceptions of Stakeholders Involved in Vector Control and Vector-Borne Disease Research and Surveillance in Orinoquia, Colombia. Trop Med Infect Dis 2024; 9:43. [PMID: 38393132 PMCID: PMC10892243 DOI: 10.3390/tropicalmed9020043] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/31/2023] [Revised: 12/16/2023] [Accepted: 12/20/2023] [Indexed: 02/25/2024] Open
Abstract
Colombia has a tropical climate and environmental conditions that favour the circulation of most of the known vector-borne diseases (VBDs). Protocols have been established and implemented to address the threats of these diseases, but they are for country-wide use and do not take into consideration the nuances of the different environments of the country. Almost the entire population is vulnerable to infection with one or more VBD. This study aims to characterise the perceptions and experiences of stakeholders involved in vector control and VBDs in the Orinoquia region in Colombia. Two panel discussions, and 12 semi-structured interviews, were conducted. Experts from the Colombian National Health Institute (INS), health secretaries from Meta, Guaviare and Vichada Departments, academic researchers, and individuals from private vector control companies participated. All sessions were recorded, transcribed, and translated, and then subject to thematic analysis. Three major themes emerged: involvement, limitations, and recommendations. Results showed that participants are engaged in vector surveillance activities, education, and vector control research. Participants focused on problems of disjointed efforts towards VBD control between health secretaries and the health ministry, as well as societal issues, such as socioeconomic, cultural, and political issues, which became the rationale for the lack of vector control resources. Responses in the panel discussions and interviews overlapped in opinions, and suggested that vector control could be improved through better communication between vector control bodies, strengthened engagement with vulnerable communities, more collaborative actions, and a more balanced distribution of resources.
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Affiliation(s)
| | - Maria Claudelle Tacugue
- Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
| | - Grace M Power
- Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
- MRC Integrative Epidemiology Unit, Population Health Sciences, Bristol Medical School, University of Bristol, Bristol BS8 1QU, UK
| | - Rimsha Qureshi
- Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
| | - Frederik Seelig
- Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
- Global Vector Hub, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
| | - Juliana Quintero
- Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
- Division of Population Health and Internal Medicine, Fundación Santa Fe de Bogotá, Bogotá 110011, Colombia
| | - James G Logan
- Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
| | - Robert T Jones
- Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
- Global Vector Hub, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
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41
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Yin C, Morita T, Parrish JZ. A cell atlas of the larval Aedes aegypti ventral nerve cord. Neural Dev 2024; 19:2. [PMID: 38297398 PMCID: PMC10829479 DOI: 10.1186/s13064-023-00178-8] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/23/2023] [Accepted: 11/28/2023] [Indexed: 02/02/2024] Open
Abstract
Mosquito-borne diseases account for nearly 1 million human deaths annually, yet we have a limited understanding of developmental events that influence host-seeking behavior and pathogen transmission in mosquitoes. Mosquito-borne pathogens are transmitted during blood meals, hence adult mosquito behavior and physiology have been intensely studied. However, events during larval development shape adult traits, larvae respond to many of the same sensory cues as adults, and larvae are susceptible to infection by many of the same disease-causing agents as adults. Hence, a better understanding of larval physiology will directly inform our understanding of physiological processes in adults. Here, we use single cell RNA sequencing (scRNA-seq) to provide a comprehensive view of cellular composition in the Aedes aegypti larval ventral nerve cord (VNC), a central hub of sensory inputs and motor outputs which additionally controls multiple aspects of larval physiology. We identify more than 35 VNC cell types defined in part by neurotransmitter and neuropeptide expression. We also explore diversity among monoaminergic and peptidergic neurons that likely control key elements of larval physiology and developmental timing, and identify neuroblasts and immature neurons, providing a view of neuronal differentiation in the VNC. Finally, we find that larval cell composition, number, and position are preserved in the adult abdominal VNC, suggesting studies of larval VNC form and function will likely directly inform our understanding adult mosquito physiology. Altogether, these studies provide a framework for targeted analysis of VNC development and neuronal function in Aedes aegypti larvae.
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Affiliation(s)
- Chang Yin
- Department of Biology, University of Washington, Seattle, WA, 98195, USA
- Division of Education, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA, 02543, USA
| | - Takeshi Morita
- Division of Education, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA, 02543, USA
- Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY, 10065, USA
- Howard Hughes Medical Institute, New York, NY, 10065, USA
| | - Jay Z Parrish
- Department of Biology, University of Washington, Seattle, WA, 98195, USA.
- Division of Education, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA, 02543, USA.
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Couper LI, Farner JE, Lyberger KP, Lee AS, Mordecai EA. Mosquito thermal tolerance is remarkably constrained across a large climatic range. Proc Biol Sci 2024; 291:20232457. [PMID: 38264779 PMCID: PMC10806440 DOI: 10.1098/rspb.2023.2457] [Citation(s) in RCA: 10] [Impact Index Per Article: 10.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/03/2023] [Accepted: 12/15/2023] [Indexed: 01/25/2024] Open
Abstract
How mosquitoes may respond to rapid climate warming remains unknown for most species, but will have major consequences for their future distributions, with cascading impacts on human well-being, biodiversity and ecosystem function. We investigated the adaptive potential of a wide-ranging mosquito species, Aedes sierrensis, across a large climatic gradient by conducting a common garden experiment measuring the thermal limits of mosquito life-history traits. Although field-collected populations originated from vastly different thermal environments that spanned over 1200 km, we found limited variation in upper thermal tolerance between populations. In particular, the upper thermal limits of all life-history traits varied by less than 3°C across the species range and, for most traits, did not differ significantly between populations. For one life-history trait-pupal development rate-we did detect significant variation in upper thermal limits between populations, and this variation was strongly correlated with source temperatures, providing evidence of local thermal adaptation for pupal development. However, we found that maximum environmental temperatures across most of the species' range already regularly exceed the highest upper thermal limits estimated under constant temperatures. This result suggests that strategies for coping with and/or avoiding thermal extremes are likely key components of current and future mosquito thermal tolerance.
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Affiliation(s)
- Lisa I. Couper
- Department of Biology, Stanford University, 327 Campus Drive, Stanford, CA 94305, USA
| | - Johannah E. Farner
- Department of Biology, Stanford University, 327 Campus Drive, Stanford, CA 94305, USA
| | - Kelsey P. Lyberger
- Department of Biology, Stanford University, 327 Campus Drive, Stanford, CA 94305, USA
| | - Alexandra S. Lee
- Department of Biology, Stanford University, 327 Campus Drive, Stanford, CA 94305, USA
| | - Erin A. Mordecai
- Department of Biology, Stanford University, 327 Campus Drive, Stanford, CA 94305, USA
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43
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Colston JM. Elucidating the Impacts of Climate on Dengue Transmission Through Mathematical Models: New Evidence From a Recent Outbreak on the Island of Réunion. J Infect Dis 2024; 229:1-3. [PMID: 37988607 DOI: 10.1093/infdis/jiad473] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/23/2023] Open
Affiliation(s)
- Josh M Colston
- Division of Infectious Diseases and International Health, University of Virginia School of Medicine, 345 Crispell Drive, Building MR-6, Charlottesville, Virginia
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Andronico A, Menudier L, Salje H, Vincent M, Paireau J, de Valk H, Gallian P, Pastorino B, Brady O, de Lamballerie X, Lazarus C, Paty MC, Vilain P, Noel H, Cauchemez S. Comparing the Performance of Three Models Incorporating Weather Data to Forecast Dengue Epidemics in Reunion Island, 2018-2019. J Infect Dis 2024; 229:10-18. [PMID: 37988167 PMCID: PMC10786251 DOI: 10.1093/infdis/jiad468] [Citation(s) in RCA: 4] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/12/2023] [Accepted: 10/27/2023] [Indexed: 11/23/2023] Open
Abstract
We developed mathematical models to analyze a large dengue virus (DENV) epidemic in Reunion Island in 2018-2019. Our models captured major drivers of uncertainty including the complex relationship between climate and DENV transmission, temperature trends, and underreporting. Early assessment correctly concluded that persistence of DENV transmission during the austral winter 2018 was likely and that the second epidemic wave would be larger than the first one. From November 2018, the detection probability was estimated at 10%-20% and, for this range of values, our projections were found to be remarkably accurate. Overall, we estimated that 8% and 18% of the population were infected during the first and second wave, respectively. Out of the 3 models considered, the best-fitting one was calibrated to laboratory entomological data, and accounted for temperature but not precipitation. This study showcases the contribution of modeling to strengthen risk assessments and planning of national and local authorities.
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Affiliation(s)
- Alessio Andronico
- Mathematical Modelling of Infectious Diseases Unit, Institut Pasteur, Université Paris Cité, UMR2000, CNRS, Paris, France
| | - Luce Menudier
- Regional Unit Saint-Denis de la Réunion, French Public Health Agency, Saint-Denis, Réunion Island, France
| | - Henrik Salje
- Department of Genetics, University of Cambridge, Cambridge, United Kingdom
| | - Muriel Vincent
- Regional Unit Saint-Denis de la Réunion, French Public Health Agency, Saint-Denis, Réunion Island, France
| | - Juliette Paireau
- Mathematical Modelling of Infectious Diseases Unit, Institut Pasteur, Université Paris Cité, UMR2000, CNRS, Paris, France
- Infectious Diseases Department, French Public Health Agency, Saint-Maurice, France
| | - Henriette de Valk
- Vectorborn, Foodborn and Zoonotic Infections Department, French Public Health Agency, Saint-Maurice, France
| | - Pierre Gallian
- Etablissement Français du Sang Provence Alpes Côte d'Azur et Corse, Marseille, France
- Unité des Virus Émergents, Aix-Marseille University, IRD 190, Inserm 1207, Marseille, France
| | - Boris Pastorino
- Unité des Virus Émergents, Aix-Marseille University, IRD 190, Inserm 1207, Marseille, France
| | - Oliver Brady
- Centre for the Mathematical Modelling of Infectious Disease, London School of Hygiene and Tropical Medicine, London, United Kingdom
- Department of Infectious Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, United Kingdom
| | - Xavier de Lamballerie
- Unité des Virus Émergents, Aix-Marseille University, IRD 190, Inserm 1207, Marseille, France
| | - Clément Lazarus
- Division of Surveillance and Health Security, Directorate General for Health, Ministry of Health, Paris, France
| | - Marie-Claire Paty
- Vectorborn, Foodborn and Zoonotic Infections Department, French Public Health Agency, Saint-Maurice, France
| | - Pascal Vilain
- Regional Unit Saint-Denis de la Réunion, French Public Health Agency, Saint-Denis, Réunion Island, France
| | - Harold Noel
- Vectorborn, Foodborn and Zoonotic Infections Department, French Public Health Agency, Saint-Maurice, France
| | - Simon Cauchemez
- Mathematical Modelling of Infectious Diseases Unit, Institut Pasteur, Université Paris Cité, UMR2000, CNRS, Paris, France
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Celone M, Beeman S, Han BA, Potter AM, Pecor DB, Okech B, Pollett S. Understanding transmission risk and predicting environmental suitability for Mayaro Virus in Central and South America. PLoS Negl Trop Dis 2024; 18:e0011859. [PMID: 38194417 PMCID: PMC10775973 DOI: 10.1371/journal.pntd.0011859] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/10/2023] [Accepted: 12/12/2023] [Indexed: 01/11/2024] Open
Abstract
Mayaro virus (MAYV) is a mosquito-borne Alphavirus that is widespread in South America. MAYV infection often presents with non-specific febrile symptoms but may progress to debilitating chronic arthritis or arthralgia. Despite the pandemic threat of MAYV, its true distribution remains unknown. The objective of this study was to clarify the geographic distribution of MAYV using an established risk mapping framework. This consisted of generating evidence consensus scores for MAYV presence, modeling the potential distribution of MAYV in select countries across Central and South America, and estimating the population residing in areas suitable for MAYV transmission. We compiled a georeferenced compendium of MAYV occurrence in humans, animals, and arthropods. Based on an established evidence consensus framework, we integrated multiple information sources to assess the total evidence supporting ongoing transmission of MAYV within each country in our study region. We then developed high resolution maps of the disease's estimated distribution using a boosted regression tree approach. Models were developed using nine climatic and environmental covariates that are related to the MAYV transmission cycle. Using the output of our boosted regression tree models, we estimated the total population living in regions suitable for MAYV transmission. The evidence consensus scores revealed high or very high evidence of MAYV transmission in several countries including Brazil (especially the states of Mato Grosso and Goiás), Venezuela, Peru, Trinidad and Tobago, and French Guiana. According to the boosted regression tree models, a substantial region of South America is suitable for MAYV transmission, including north and central Brazil, French Guiana, and Suriname. Some regions (e.g., Guyana) with only moderate evidence of known transmission were identified as highly suitable for MAYV. We estimate that approximately 58.9 million people (95% CI: 21.4-100.4) in Central and South America live in areas that may be suitable for MAYV transmission, including 46.2 million people (95% CI: 17.6-68.9) in Brazil. Our results may assist in prioritizing high-risk areas for vector control, human disease surveillance and ecological studies.
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Affiliation(s)
- Michael Celone
- Department of Preventive Medicine & Biostatistics, Uniformed Services University of the Health Sciences, F. Edward Hébert School of Medicine, Bethesda, Maryland, United States of America
| | - Sean Beeman
- Department of Preventive Medicine & Biostatistics, Uniformed Services University of the Health Sciences, F. Edward Hébert School of Medicine, Bethesda, Maryland, United States of America
| | - Barbara A. Han
- Cary Institute of Ecosystem Studies, Millbrook, New York, United States of America
| | - Alexander M. Potter
- One Health Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America
- Walter Reed Biosystematics Unit, Smithsonian Museum Support Center, Suitland, Maryland, United States of America
- Department of Entomology, Smithsonian Institution—National Museum of Natural History (NMNH), Washington, DC, United States of America
| | - David B. Pecor
- One Health Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America
- Walter Reed Biosystematics Unit, Smithsonian Museum Support Center, Suitland, Maryland, United States of America
- Department of Entomology, Smithsonian Institution—National Museum of Natural History (NMNH), Washington, DC, United States of America
| | - Bernard Okech
- Department of Preventive Medicine & Biostatistics, Uniformed Services University of the Health Sciences, F. Edward Hébert School of Medicine, Bethesda, Maryland, United States of America
| | - Simon Pollett
- Infectious Disease Clinical Research Program, Department of Preventive Medicine and Biostatistics, Uniformed Services University of the Health Sciences, Bethesda, Maryland, United States of America
- Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., Bethesda, Maryland, United States of America
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46
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Dennington NL, Grossman MK, Ware-Gilmore F, Teeple JL, Johnson LR, Shocket MS, McGraw EA, Thomas MB. Phenotypic adaptation to temperature in the mosquito vector, Aedes aegypti. GLOBAL CHANGE BIOLOGY 2024; 30:e17041. [PMID: 38273521 DOI: 10.1111/gcb.17041] [Citation(s) in RCA: 7] [Impact Index Per Article: 7.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/21/2023] [Revised: 10/24/2023] [Accepted: 10/28/2023] [Indexed: 01/27/2024]
Abstract
Most models exploring the effects of climate change on mosquito-borne disease ignore thermal adaptation. However, if local adaptation leads to changes in mosquito thermal responses, "one size fits all" models could fail to capture current variation between populations and future adaptive responses to changes in temperature. Here, we assess phenotypic adaptation to temperature in Aedes aegypti, the primary vector of dengue, Zika, and chikungunya viruses. First, to explore whether there is any difference in existing thermal response of mosquitoes between populations, we used a thermal knockdown assay to examine five populations of Ae. aegypti collected from climatically diverse locations in Mexico, together with a long-standing laboratory strain. We identified significant phenotypic variation in thermal tolerance between populations. Next, to explore whether such variation can be generated by differences in temperature, we conducted an experimental passage study by establishing six replicate lines from a single field-derived population of Ae. aegypti from Mexico, maintaining half at 27°C and the other half at 31°C. After 10 generations, we found a significant difference in mosquito performance, with the lines maintained under elevated temperatures showing greater thermal tolerance. Moreover, these differences in thermal tolerance translated to shifts in the thermal performance curves for multiple life-history traits, leading to differences in overall fitness. Together, these novel findings provide compelling evidence that Ae. aegypti populations can and do differ in thermal response, suggesting that simplified thermal performance models might be insufficient for predicting the effects of climate on vector-borne disease transmission.
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Affiliation(s)
- Nina L Dennington
- Department of Entomology, The Pennsylvania State University, University Park, Pennsylvania, USA
- The Center for Infectious Disease Dynamics, The Huck Life Sciences, The Pennsylvania State University, University Park, Pennsylvania, USA
| | - Marissa K Grossman
- Department of Entomology, The Pennsylvania State University, University Park, Pennsylvania, USA
| | - Fhallon Ware-Gilmore
- Department of Entomology, The Pennsylvania State University, University Park, Pennsylvania, USA
- The Center for Infectious Disease Dynamics, The Huck Life Sciences, The Pennsylvania State University, University Park, Pennsylvania, USA
| | - Janet L Teeple
- Department of Entomology, The Pennsylvania State University, University Park, Pennsylvania, USA
| | - Leah R Johnson
- Department of Statistics, Virginia Tech, Blacksburg, Virginia, USA
| | - Marta S Shocket
- Department of Geography, University of Florida, Gainesville, Florida, USA
- Lancaster Environment Centre, Lancaster University, Lancaster, UK
| | - Elizabeth A McGraw
- The Center for Infectious Disease Dynamics, The Huck Life Sciences, The Pennsylvania State University, University Park, Pennsylvania, USA
- Department of Biology, The Pennsylvania State University, University Park, Pennsylvania, USA
| | - Matthew B Thomas
- Department of Entomology and Nematology, University of Florida, Gainesville, Florida, USA
- Invasion Science Research Institute, University of Florida, Gainesville, Florida, USA
- Department of Biology, University of York, York, UK
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47
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Wang YR, Samset BH, Stordal F, Bryn A, Hessen DO. Past and future trends of diurnal temperature range and their correlation with vegetation assessed by MODIS and CMIP6. THE SCIENCE OF THE TOTAL ENVIRONMENT 2023; 904:166727. [PMID: 37673261 DOI: 10.1016/j.scitotenv.2023.166727] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/21/2023] [Revised: 08/22/2023] [Accepted: 08/29/2023] [Indexed: 09/08/2023]
Abstract
Temperature anomalies and changes in the diurnal temperature range (DTR) are expected to pose physiological challenges to biota; hence, both spatial and temporal variations in DTR provide important insights into temperature-induced stress in humans, animals, and vegetation. Furthermore, vegetation could dampen temperature variability. Here, we use the Moderate Resolution Imaging Spectroradiometer (MODIS) remote sensing data of Land Surface Temperature (LST) to evaluate the global variation in DTR and its rate of change in spatial and temporal scales for the two decades spanning from 2001 to 2020. We show that North America, Africa, and Antarctica, as well as the global mean, experienced statistically significant DTR rates of change over the last 20 years in either summer, winter, or the annual mean. The rates were all negative, indicating the day-night temperature differences are decreasing in those regions because night temperatures are increasing at a faster rate than day temperatures. MODIS data of the Normalized Difference Vegetation Index (NDVI) revealed a strongly negative correlation with DTR, with a spatial correlation coefficient of -0.61. This correlation demonstrates a prominent dampening effect of vegetation on diurnal temperature oscillations. For future DTR projections, we used 19 models in the Coupled Model Intercomparison Project 6 (CMIP6) to predict global DTR trends from 2021 to 2050 with low and high CO2 concentration scenarios. The high CO2 emission scenario projects significant decreases in DTR in circumpolar regions, central Africa, and India compared to the low CO2 scenario. This difference in the two scenarios underscores the substantial influence of increased global temperatures and elevated CO2 concentration on DTR and, consequently, on the ecosystems in certain regions.
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Affiliation(s)
- You-Ren Wang
- Dept. Marine Environment and Engineering, National Sun Yat-sen University, Kaohsiung 80424, Taiwan; Graduate Institute of Marine Affairs, National Sun Yat-sen University, Kaohsiung 80424, Taiwan; Dept. Biosciences and Centre for Biogeochemistry in the Anthropocene, University of Oslo, Oslo 0316, Norway.
| | - Bjørn H Samset
- CICERO Center for International Climate Research, Oslo 0349, Norway
| | - Frode Stordal
- Dept. Geosciences and Centre for Biogeochemistry in the Anthropocene, University of Oslo, Oslo 0316, Norway
| | - Anders Bryn
- Natural History Museum and Centre for Biogeochemistry in the Anthropocene, University of Oslo, Oslo 0316, Norway
| | - Dag O Hessen
- Dept. Biosciences and Centre for Biogeochemistry in the Anthropocene, University of Oslo, Oslo 0316, Norway
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48
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Athni TS, Childs ML, Glidden CK, Mordecai EA. Temperature dependence of mosquitoes: comparing mechanistic and machine learning approaches. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2023:2023.12.04.569955. [PMID: 38105988 PMCID: PMC10723351 DOI: 10.1101/2023.12.04.569955] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/19/2023]
Abstract
Mosquito vectors of pathogens (e.g., Aedes , Anopheles , and Culex spp. which transmit dengue, Zika, chikungunya, West Nile, malaria, and others) are of increasing concern for global public health. These vectors are geographically shifting under climate and other anthropogenic changes. As small-bodied ectotherms, mosquitoes are strongly affected by temperature, which causes unimodal responses in mosquito life history traits (e.g., biting rate, adult mortality rate, mosquito development rate, and probability of egg-to-adult survival) that exhibit upper and lower thermal limits and intermediate thermal optima in laboratory studies. However, it remains unknown how mosquito thermal responses measured in laboratory experiments relate to the realized thermal responses of mosquitoes in the field. To address this gap, we leverage thousands of global mosquito occurrences and geospatial satellite data at high spatial resolution to construct machine-learning based species distribution models, from which vector thermal responses are estimated. We apply methods to restrict models to the relevant mosquito activity season and to conduct ecologically-plausible spatial background sampling centered around ecoregions for comparison to mosquito occurrence records. We found that thermal minima estimated from laboratory studies were highly correlated with those from the species distributions (r = 0.90). The thermal optima were less strongly correlated (r = 0.69). For most species, we did not detect thermal maxima from their observed distributions so were unable to compare to laboratory-based estimates. The results suggest that laboratory studies have the potential to be highly transportable to predicting lower thermal limits and thermal optima of mosquitoes in the field. At the same time, lab-based models likely capture physiological limits on mosquito persistence at high temperatures that are not apparent from field-based observational studies but may critically determine mosquito responses to climate warming.
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49
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Couper LI, Farner JE, Lyberger KP, Lee AS, Mordecai EA. Mosquito thermal tolerance is remarkably constrained across a large climatic range. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2023:2023.03.02.530886. [PMID: 37961581 PMCID: PMC10634975 DOI: 10.1101/2023.03.02.530886] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/15/2023]
Abstract
How mosquitoes may respond to rapid climate warming remains unknown for most species, but will have major consequences for their future distributions, with cascading impacts on human well-being, biodiversity, and ecosystem function. We investigated the adaptive potential of a wide-ranging mosquito species, Aedes sierrensis, across a large climatic gradient by conducting a common garden experiment measuring the thermal limits of mosquito life history traits. Although field-collected populations originated from vastly different thermal environments that spanned over 1,200 km, we found remarkably limited variation in upper thermal tolerance between populations, with the upper thermal limits of fitness varying by <1°C across the species range. For one life history trait-pupal development rate-we did detect significant variation in upper thermal limits between populations, and this variation was strongly correlated with source temperatures, providing evidence of local thermal adaptation for pupal development. However, we found environmental temperatures already regularly exceed our highest estimated upper thermal limits throughout most of the species range, suggesting limited potential for mosquito thermal tolerance to evolve on pace with warming. Strategies for avoiding high temperatures such as diapause, phenological shifts, and behavioral thermoregulation are likely important for mosquito persistence.
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Affiliation(s)
- Lisa I. Couper
- Department of Biology, Stanford University. 327 Campus Drive, Stanford CA 94305
| | - Johannah E. Farner
- Department of Biology, Stanford University. 327 Campus Drive, Stanford CA 94305
| | - Kelsey P. Lyberger
- Department of Biology, Stanford University. 327 Campus Drive, Stanford CA 94305
| | - Alexandra S. Lee
- Department of Biology, Stanford University. 327 Campus Drive, Stanford CA 94305
| | - Erin A. Mordecai
- Department of Biology, Stanford University. 327 Campus Drive, Stanford CA 94305
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50
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Ouattara CA, Traore TI, Ouedraogo B, Sylla B, Traore S, Meda CZ, Sangare I, Savadogo LBG. Spatio-Temporal Determinants of Dengue Epidemics in the Central Region of Burkina Faso. Trop Med Infect Dis 2023; 8:482. [PMID: 37999601 PMCID: PMC10675449 DOI: 10.3390/tropicalmed8110482] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/28/2023] [Revised: 10/22/2023] [Accepted: 10/24/2023] [Indexed: 11/25/2023] Open
Abstract
The aim of this study was to analyze the spatio-temporal distribution and determinants of the 2017 dengue epidemic in Burkina Faso. A principal component analysis of meteorological and environmental factors was performed to reduce dimensions and avoid collinearities. An initial generalized additive model assessed the impact of the components derived from this analysis on dengue incidence. Dengue incidence increased mainly with relative humidity, precipitation, normalized difference vegetation index and minimum temperature with an 8-week lag. A Kulldoff Satscan scan was used to identify high-risk dengue clusters, and a second generalized additive model assessed the risk of a health area being at high risk according to land-use factors. The spatio-temporal distribution of dengue fever was heterogeneous and strongly correlated with meteorological factors. The rural communes of Sabaa and Koubri were the areas most at risk. This study provides useful information for planning targeted dengue control strategies in Burkina Faso.
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Affiliation(s)
- Cheick Ahmed Ouattara
- Doctoral School of Health Sciences, Nazi Boni University, Bobo-Dioulasso 1091, Burkina Faso;
| | - Tiandiogo Isidore Traore
- Higher Institute of Health Sciences, Nazi Boni University, Bobo-Dioulasso 1091, Burkina Faso; (T.I.T.); (C.Z.M.); (I.S.); (L.B.G.S.)
| | - Boukary Ouedraogo
- Directorate of Health Information Systems, Ministry of Health, Ouagadougou 7009, Burkina Faso; (B.O.); (B.S.)
| | - Bry Sylla
- Directorate of Health Information Systems, Ministry of Health, Ouagadougou 7009, Burkina Faso; (B.O.); (B.S.)
| | - Seydou Traore
- Doctoral School of Health Sciences, Nazi Boni University, Bobo-Dioulasso 1091, Burkina Faso;
| | - Clement Ziemle Meda
- Higher Institute of Health Sciences, Nazi Boni University, Bobo-Dioulasso 1091, Burkina Faso; (T.I.T.); (C.Z.M.); (I.S.); (L.B.G.S.)
| | - Ibrahim Sangare
- Higher Institute of Health Sciences, Nazi Boni University, Bobo-Dioulasso 1091, Burkina Faso; (T.I.T.); (C.Z.M.); (I.S.); (L.B.G.S.)
| | - Leon Blaise G. Savadogo
- Higher Institute of Health Sciences, Nazi Boni University, Bobo-Dioulasso 1091, Burkina Faso; (T.I.T.); (C.Z.M.); (I.S.); (L.B.G.S.)
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