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Eloise B. Stephenson
Biology Department, Stanford University, Stanford, CA 94305, USA

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Review
Published: 09 February 2021 in Viruses
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Mosquito-borne viruses are well recognized as a global public health burden amongst humans, but the effects on non-human vertebrates is rarely reported. Australia, houses a number of endemic mosquito-borne viruses, such as Ross River virus, Barmah Forest virus, and Murray Valley encephalitis virus. In this review, we synthesize the current state of mosquito-borne viruses impacting non-human vertebrates in Australia, including diseases that could be introduced due to local mosquito distribution. Given the unique island biogeography of Australia and the endemism of vertebrate species (including macropods and monotremes), Australia is highly susceptible to foreign mosquito species becoming established, and mosquito-borne viruses becoming endemic alongside novel reservoirs. For each virus, we summarize the known geographic distribution, mosquito vectors, vertebrate hosts, clinical signs and treatments, and highlight the importance of including non-human vertebrates in the assessment of future disease outbreaks. The mosquito-borne viruses discussed can impact wildlife, livestock, and companion animals, causing significant changes to Australian ecology and economy. The complex nature of mosquito-borne disease, and challenges in assessing the impacts to non-human vertebrate species, makes this an important topic to periodically review.

ACS Style

Oselyne Ong; Eloise Skinner; Brian Johnson; Julie Old. Mosquito-Borne Viruses and Non-Human Vertebrates in Australia: A Review. Viruses 2021, 13, 265 .

AMA Style

Oselyne Ong, Eloise Skinner, Brian Johnson, Julie Old. Mosquito-Borne Viruses and Non-Human Vertebrates in Australia: A Review. Viruses. 2021; 13 (2):265.

Chicago/Turabian Style

Oselyne Ong; Eloise Skinner; Brian Johnson; Julie Old. 2021. "Mosquito-Borne Viruses and Non-Human Vertebrates in Australia: A Review." Viruses 13, no. 2: 265.

Preprint content
Published: 28 January 2021
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Identifying the key vector and host species driving transmission is notoriously difficult for vector-borne zoonoses, but critical for disease control. Here, we present a general approach for quantifying the role hosts and vectors play in transmission that integrates species’ physiological competence with their ecological traits. We apply this model to the medically important arbovirus Ross River virus (RRV), in Brisbane, Australia. We found that vertebrate species with high physiological competence weren’t the most important for community transmission. Instead, we estimated that humans (previously overlooked as epidemiologically important hosts) potentially play an important role in RRV transmission, in part, because highly competent vectors readily feed on them and are highly abundant. By contrast, vectors with high physiological competence were also important for community transmission. Finally, we uncovered two potential transmission cycles: an enzootic cycle involving birds and an urban cycle involving humans. This modelling approach has direct application to other zoonotic arboviruses.

ACS Style

Morgan P. Kain; Eloise B. Skinner; Andrew F. Van Den Hurk; Hamish McCallum; Erin A. Mordecai. Physiology and ecology together regulate host and vector importance for Ross River virus and other vector-borne diseases. 2021, 1 .

AMA Style

Morgan P. Kain, Eloise B. Skinner, Andrew F. Van Den Hurk, Hamish McCallum, Erin A. Mordecai. Physiology and ecology together regulate host and vector importance for Ross River virus and other vector-borne diseases. . 2021; ():1.

Chicago/Turabian Style

Morgan P. Kain; Eloise B. Skinner; Andrew F. Van Den Hurk; Hamish McCallum; Erin A. Mordecai. 2021. "Physiology and ecology together regulate host and vector importance for Ross River virus and other vector-borne diseases." , no. : 1.

Micro article
Published: 27 November 2020 in MethodsX
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Over the last decade, an arbovirus surveillance system based on the preservation of nucleic acids (RNA/DNA) has been developed using Flinders Technology Associates (FTA®) cards. Soaked in honey, FTA® cards are applied in the field to detect arboviruses excreted during mosquito sugar feeding. This technique has been shown to be inexpensive and efficient, and the implementation of this system for detecting parasites could be of international importance. As Leishmania parasites are highly prevalent in developing countries, FTA® cards may offer an alternative inexpensive tool to enhance field surveillance activities for leishmaniasis. Not only will the simple approach of applying the cards in programs substitute the necessary extensive training of personnel, it can preclude the need to screen large samples and analysis of insect populations to provide evidence of disease transmission. In our hands, Leishmania macropodum DNA was shown to be stable on FTA® cards during a 10-week time course, supporting their suitability for projects where direct access to laboratories is unobtainable and samples require storage prior to processing. This may benefit programs in remote areas where accessibility to laboratory facilities are limited and samples need to be stored long-term. Overall, this study found that FTA® cards are a valuable tool in the surveillance of leishmaniasis. Download : Download high-res image (139KB)Download : Download full-size image

ACS Style

Elina Panahi; Martin Shivas; Sonja Hall-Mendelin; Nina Kurucz; Penny A. Rudd; Rachel De Araujo; Eloise B. Skinner; Lorna Melville; Lara J. Herrero. Utilising a novel surveillance system to enhance field screening activities for the leishmaniases. MethodsX 2020, 7, 101156 .

AMA Style

Elina Panahi, Martin Shivas, Sonja Hall-Mendelin, Nina Kurucz, Penny A. Rudd, Rachel De Araujo, Eloise B. Skinner, Lorna Melville, Lara J. Herrero. Utilising a novel surveillance system to enhance field screening activities for the leishmaniases. MethodsX. 2020; 7 ():101156.

Chicago/Turabian Style

Elina Panahi; Martin Shivas; Sonja Hall-Mendelin; Nina Kurucz; Penny A. Rudd; Rachel De Araujo; Eloise B. Skinner; Lorna Melville; Lara J. Herrero. 2020. "Utilising a novel surveillance system to enhance field screening activities for the leishmaniases." MethodsX 7, no. : 101156.

Journal article
Published: 01 September 2020 in Vector-Borne and Zoonotic Diseases
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Transmission of vector-borne pathogens can vary in complexity from single-vector, single-host systems through to multivector, multihost vertebrate systems. Understanding the dynamics of transmission is important for disease prevention efforts, but is dependent on disentangling complex interactions within coupled natural systems. Ross River virus (RRV) is a multivector multihost pathogen responsible for the greatest number of notified vector-borne pathogen infections in humans in Australia. Current evidence suggests that nonhuman vertebrates are critical for the maintenance and spillover of RRV into mosquito populations. Yet, there is a limited knowledge of which mosquito vector species and amplifying vertebrate host species are most important for transmission of RRV to humans. We conducted field surveys of nonhuman vertebrates and mosquitoes in the RRV endemic city of Brisbane, Australia, to assess the effect of vector and host community structure on human RRV notifications. Six suburbs were selected across a gradient of human disease notification rates. Differences in vertebrate and mosquito compositions were observed across all suburbs. Suburbs with higher RRV notification rates contained greater vertebrate biomass (dominated by the presence of horses) and higher mosquito abundances. This study suggests that horse–mosquito interactions should be considered in more detail and that vertebrate biomass and mosquito abundance be incorporated into future RRV modeling studies and considered in public health strategies for RRV management.

ACS Style

Eloise B. Skinner; Amanda Murphy; Cassie C. Jansen; Martin A. Shivas; Hamish McCallum; Michael B. Onn; Simon A. Reid; Alison J. Peel. Associations Between Ross River Virus Infection in Humans and Vector-Vertebrate Community Ecology in Brisbane, Australia. Vector-Borne and Zoonotic Diseases 2020, 20, 680 -691.

AMA Style

Eloise B. Skinner, Amanda Murphy, Cassie C. Jansen, Martin A. Shivas, Hamish McCallum, Michael B. Onn, Simon A. Reid, Alison J. Peel. Associations Between Ross River Virus Infection in Humans and Vector-Vertebrate Community Ecology in Brisbane, Australia. Vector-Borne and Zoonotic Diseases. 2020; 20 (9):680-691.

Chicago/Turabian Style

Eloise B. Skinner; Amanda Murphy; Cassie C. Jansen; Martin A. Shivas; Hamish McCallum; Michael B. Onn; Simon A. Reid; Alison J. Peel. 2020. "Associations Between Ross River Virus Infection in Humans and Vector-Vertebrate Community Ecology in Brisbane, Australia." Vector-Borne and Zoonotic Diseases 20, no. 9: 680-691.

Journal article
Published: 17 June 2020 in International Journal for Parasitology: Parasites and Wildlife
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Up until recently, Australia was considered free of Leishmania due to the absence of phlebotomine sandfly species (Diptera: Phlebotominae) known to transmit Leishmania parasites in other parts of the world. The discovery of Leishmania (Mundinia) macropodum (Kinetoplastida: Trypanosomatidae) in Northern Australia sparked questions as to the existence of alternative vectors of Leishmania. This has added to the complexity of fully understanding the parasite's interaction with its vector, which is known to be very specific. Previous findings demonstrated L. macropodum infection beyond the blood meal stage in the day-biting midges Forcipomyia (Lasiohelea) Kieffer (Diptera: Ceratopogonidae) implicating them in the parasite's life cycle. Currently, there is no conclusive evidence demonstrating this suspected vector to transmit L. macropodum to a naïve host. Therefore, this research aimed to investigate the vector competency of day-biting midge F. (Lasiohelea) to transmit L. macropodum utilising a novel technology that preserves nucleic acids. Honey-soaked Flinders Technology Associates (FTA®) filter-paper cards were used to obtain saliva expectorated from biting midges while sugar-feeding. F. (Lasiohelea) were aspirated directly off macropods from a known Leishmania-transmission site and were kept in a waxed-paper container holding a honey-coated FTA® card for feeding. Insect identification and Taqman quantitative real-time PCR (qPCR) screening assays revealed L. macropodum DNA in F. (Lasiohelea) up to 7 days post field-collection, and in an unidentified biting midge, previously known as F. (Lasiohelea) sp.1. Moreover, 7/145 (4.83%) of FTA® cards were confirmed positive with L. macropodum DNA after exposure to field-collected F. (Lasiohelea). Additionally, FTA® cards were found to be a valuable surveillance tool, given the ease of use in the field and laboratory. Overall, our findings support previous reports on L. macropodum transmission by an alternative vector to phlebotomine sandflies. Further studies identifying and isolating infective L. macropodum promastigotes is necessary to resolve questions on the L. macropodum vector.

ACS Style

Elina Panahi; Martin Shivas; Sonja Hall-Mendelin; Nina Kurucz; Penny A. Rudd; Rachel De Araujo; Eloise B. Skinner; Lorna Melville; Lara J. Herrero. Utilising a novel surveillance system to investigate species of Forcipomyia (Lasiohelea) (Diptera: Ceratopogonidae) as the suspected vectors of Leishmania macropodum (Kinetoplastida: Trypanosomatidae) in the Darwin region of Australia. International Journal for Parasitology: Parasites and Wildlife 2020, 12, 192 -198.

AMA Style

Elina Panahi, Martin Shivas, Sonja Hall-Mendelin, Nina Kurucz, Penny A. Rudd, Rachel De Araujo, Eloise B. Skinner, Lorna Melville, Lara J. Herrero. Utilising a novel surveillance system to investigate species of Forcipomyia (Lasiohelea) (Diptera: Ceratopogonidae) as the suspected vectors of Leishmania macropodum (Kinetoplastida: Trypanosomatidae) in the Darwin region of Australia. International Journal for Parasitology: Parasites and Wildlife. 2020; 12 ():192-198.

Chicago/Turabian Style

Elina Panahi; Martin Shivas; Sonja Hall-Mendelin; Nina Kurucz; Penny A. Rudd; Rachel De Araujo; Eloise B. Skinner; Lorna Melville; Lara J. Herrero. 2020. "Utilising a novel surveillance system to investigate species of Forcipomyia (Lasiohelea) (Diptera: Ceratopogonidae) as the suspected vectors of Leishmania macropodum (Kinetoplastida: Trypanosomatidae) in the Darwin region of Australia." International Journal for Parasitology: Parasites and Wildlife 12, no. : 192-198.

Review
Published: 11 April 2019 in Parasites & Vectors
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Mosquito-borne diseases are associated with major global health burdens. Aedes spp. and Culex spp. are primarily responsible for the transmission of the most medically important mosquito-borne viruses, including dengue virus, West Nile virus and Zika virus. Despite the burden of these pathogens on human populations, the interactions between viruses and their mosquito hosts remain enigmatic. Viruses enter the midgut of a mosquito following the mosquito’s ingestion of a viremic blood meal. During infection, virus recognition by the mosquito host triggers their antiviral defense mechanism. Of these host defenses, activation of the RNAi pathway is the main antiviral mechanism, leading to the degradation of viral RNA, thereby inhibiting viral replication and promoting viral clearance. However, whilst antiviral host defense mechanisms limit viral replication, the mosquito immune system is unable to effectively clear the virus. As such, these viruses can establish persistent infection with little or no fitness cost to the mosquito vector, ensuring life-long transmission to humans. Understanding of the mosquito innate immune response enables the discovery of novel antivectorial strategies to block human transmission. This review provides an updated and concise summary of recent studies on mosquito antiviral immune responses, which is a key determinant for successful virus transmission. In addition, we will also discuss the factors that may contribute to persistent infection in mosquito hosts. Finally, we will discuss current mosquito transmission-blocking strategies that utilize genetically modified mosquitoes and Wolbachia-infected mosquitoes for resistance to pathogens.

ACS Style

Wai-Suet Lee; Julie A. Webster; Eugene T. Madzokere; Eloise B. Stephenson; Lara J. Herrero. Mosquito antiviral defense mechanisms: a delicate balance between innate immunity and persistent viral infection. Parasites & Vectors 2019, 12, 1 -12.

AMA Style

Wai-Suet Lee, Julie A. Webster, Eugene T. Madzokere, Eloise B. Stephenson, Lara J. Herrero. Mosquito antiviral defense mechanisms: a delicate balance between innate immunity and persistent viral infection. Parasites & Vectors. 2019; 12 (1):1-12.

Chicago/Turabian Style

Wai-Suet Lee; Julie A. Webster; Eugene T. Madzokere; Eloise B. Stephenson; Lara J. Herrero. 2019. "Mosquito antiviral defense mechanisms: a delicate balance between innate immunity and persistent viral infection." Parasites & Vectors 12, no. 1: 1-12.

Research
Published: 04 April 2019 in Parasites & Vectors
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Mosquito-borne pathogens contribute significantly to the global burden of disease, infecting millions of people each year. Mosquito feeding is critical to the transmission dynamics of pathogens, and thus it is important to understanding and interpreting mosquito feeding patterns. In this paper we explore mosquito feeding patterns and their implications for disease ecology through a meta-analysis of published blood meal results collected across Australia from more than 12,000 blood meals from 22 species. To assess mosquito-vertebrate associations and identify mosquitoes on a spectrum of generalist or specialist feeders, we analysed blood meal data in two ways; first using a novel odds ratio analysis, and secondly by calculating Shannon’s diversity scores. We find that each mosquito species had a unique feeding association with different vertebrates, suggesting species-specific feeding patterns. Broadly, mosquito species could be grouped broadly into those that were primarily ornithophilic and those that fed more often on livestock. Aggregated feeding patterns observed across Australia were not explained by intrinsic variables such as mosquito genetics or larval habitats. We discuss the implications for disease transmission by vector mosquito species classified as generalist-feeders (such as Aedes vigilax and Culex annulirostris), or specialists (such as Aedes aegypti) in light of potential influences on mosquito host choice. Overall, we find that whilst existing blood meal studies in Australia are useful for investigating mosquito feeding patterns, standardisation of blood meal study methodologies and analyses, including the incorporation of vertebrate surveys, would improve predictions of the impact of vector-host interactions on disease ecology. Our analysis can also be used as a framework to explore mosquito-vertebrate associations, in which host availability data is unavailable, in other global systems.

ACS Style

Eloise B. Stephenson; Amanda K. Murphy; Cassie C. Jansen; Alison J. Peel; Hamish McCallum. Interpreting mosquito feeding patterns in Australia through an ecological lens: an analysis of blood meal studies. Parasites & Vectors 2019, 12, 1 -11.

AMA Style

Eloise B. Stephenson, Amanda K. Murphy, Cassie C. Jansen, Alison J. Peel, Hamish McCallum. Interpreting mosquito feeding patterns in Australia through an ecological lens: an analysis of blood meal studies. Parasites & Vectors. 2019; 12 (1):1-11.

Chicago/Turabian Style

Eloise B. Stephenson; Amanda K. Murphy; Cassie C. Jansen; Alison J. Peel; Hamish McCallum. 2019. "Interpreting mosquito feeding patterns in Australia through an ecological lens: an analysis of blood meal studies." Parasites & Vectors 12, no. 1: 1-11.

Preprint
Published: 10 December 2018
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Mosquito-borne pathogens contribute significantly to the global burden of disease, infecting millions of people each year. Mosquito feeding is critical to the transmission dynamics of pathogens, and thus it is important to understanding and interpreting mosquito feeding patterns. In this paper we explore mosquito feeding patterns and their implications for disease ecology through a meta-analysis of published blood meal results collected across Australia from more than 12,000 blood meals from 22 species. To assess mosquito-vertebrate associations and identify mosquitoes on a spectrum of generalist or specialist feeders, we analysed blood meal data in two ways; first using a novel odds ratio analysis, and secondly by calculating Shannon diversity scores. We find that each mosquito species had a unique feeding association with different vertebrates, suggesting species-specific feeding patterns. Broadly, mosquito species could be grouped broadly into those that were primarily ornithophilic and those that fed more often on livestock. Aggregated feeding patterns observed across Australia were not explained by intrinsic variables such as mosquito genetics or larval habitats. We discuss the implications for disease transmission by vector mosquito species classified as generalist-feeders (such as Aedes vigilax and Culex annulirostris), or specialists (such as Aedes aegypti) in light of potential influences on mosquito host choice. Overall, we find that whilst existing blood meal studies in Australia are useful for investigating mosquito feeding patterns, standardisation of blood meal study methodologies and analyses, including the incorporation of vertebrate surveys, would improve predictions of the impact of vector-host interactions on disease ecology. Our analysis can also be used as a framework to explore mosquito-vertebrate associations, in which host availability data is unavailable, in other global systems.

ACS Style

Eloise B Stephenson; Amanda Murphy; Cassie C Jansen; Alison J Peel; Hamish McCallum. Interpreting mosquito feeding patterns in Australia through an ecological lens; an analysis of blood meal studies. 2018, 492934 .

AMA Style

Eloise B Stephenson, Amanda Murphy, Cassie C Jansen, Alison J Peel, Hamish McCallum. Interpreting mosquito feeding patterns in Australia through an ecological lens; an analysis of blood meal studies. . 2018; ():492934.

Chicago/Turabian Style

Eloise B Stephenson; Amanda Murphy; Cassie C Jansen; Alison J Peel; Hamish McCallum. 2018. "Interpreting mosquito feeding patterns in Australia through an ecological lens; an analysis of blood meal studies." , no. : 492934.

Review
Published: 19 March 2018 in Parasites & Vectors
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Understanding the non-human reservoirs of zoonotic pathogens is critical for effective disease control, but identifying the relative contributions of the various reservoirs of multi-host pathogens is challenging. For Ross River virus (RRV), knowledge of the transmission dynamics, in particular the role of non-human species, is important. In Australia, RRV accounts for the highest number of human mosquito-borne virus infections. The long held dogma that marsupials are better reservoirs than placental mammals, which are better reservoirs than birds, deserves critical review. We present a review of 50 years of evidence on non-human reservoirs of RRV, which includes experimental infection studies, virus isolation studies and serosurveys. We find that whilst marsupials are competent reservoirs of RRV, there is potential for placental mammals and birds to contribute to transmission dynamics. However, the role of these animals as reservoirs of RRV remains unclear due to fragmented evidence and sampling bias. Future investigations of RRV reservoirs should focus on quantifying complex transmission dynamics across environments.

ACS Style

Eloise B. Stephenson; Alison J. Peel; Simon A. Reid; Cassie C. Jansen; Hamish McCallum. The non-human reservoirs of Ross River virus: a systematic review of the evidence. Parasites & Vectors 2018, 11, 1 -13.

AMA Style

Eloise B. Stephenson, Alison J. Peel, Simon A. Reid, Cassie C. Jansen, Hamish McCallum. The non-human reservoirs of Ross River virus: a systematic review of the evidence. Parasites & Vectors. 2018; 11 (1):1-13.

Chicago/Turabian Style

Eloise B. Stephenson; Alison J. Peel; Simon A. Reid; Cassie C. Jansen; Hamish McCallum. 2018. "The non-human reservoirs of Ross River virus: a systematic review of the evidence." Parasites & Vectors 11, no. 1: 1-13.