Emerging Tropical Pathogens of Bats

A special issue of Tropical Medicine and Infectious Disease (ISSN 2414-6366). This special issue belongs to the section "Neglected and Emerging Tropical Diseases".

Deadline for manuscript submissions: closed (31 May 2019) | Viewed by 27170

Special Issue Editor


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Guest Editor
United States Department of Agriculture, Animal and Plant Health Inspection Service, Ames, IA, USA
Interests: rabies; emerging infectious diseases; pathogen discovery; bats; zoonotic diseases

Special Issue Information

Dear Colleagues,

During recent decades, bats (Order Chiroptera) have been increasingly recognized as reservoirs of emerging zoonotic infections, important for veterinary and public health. The majority constitute RNA-viruses including lyssaviruses, causing rabies; coronaviruses, including but not limited to the acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) related viruses; paramyxoviruses such as Hendra and Nipah, with recently recognized related paramyxoviruses (Cedar and Achimota viruses) for which zoonotic potential has to be investigated; and filoviruses. For Marburg virus, the role of the Egyptian fruit bats (Rousettus aegyptiacus) as virus reservoirs has been demonstrated via field studies and experimental sampling. However, no direct evidence supports the role of bats as reservoirs of Ebola virus. Nevertheless, a number of indirect findings (e.g., filovirus nucleic acids and filovirus-neutralizing antibodies) documented in a variety of bats in Europe and Asia support the suggestions that bats are filovirus reservoir hosts. Many other viruses from different families have been documented in bats during recent years, but their zoonotic potential and significance for veterinary service remains unclear. In addition, several bacterial pathogens have been described in bats, including bartonella, Brucella, and leptospira, which have clear zoonotic potential, but the potential role of bats as their transmitters to “terrestrial” mammals and humans needs to be elucidated. It is remarkable that the majority of these pathogens—which cause severe (frequently fatal) diseases in humans and other mammals—do not cause apparent clinical signs in bats. There may be something unique in the bat immune system in general, or in its interaction with the specific pathogens, that might evolve with other unique features of bats such as their ability of flight (associated with substantial changes in metabolism, body temperature, and DNA damage), longevity (20–30 years as documented at least for several bat species), the ability to develop torpor—either seasonal or diurnal—with the decreasing of all metabolic processes from several hours to several months.

Bats are very diverse, second only to rodents per species number among mammals (about 1200 species described to date). They are abundant in subtropical and tropical areas around the globe, occupying different ecological niches and including frugivorous, nectarivorous, insectivorous, carnivorous, and omnivorous representatives. They are social animals, forming colonies from several tens to millions of individuals, and frequently roost in close proximity to humans or agricultural animals, which provides ample opportunities for pathogen exchange. Moreover, many species of bats are migratory, and annually travel hundreds or thousands of kilometers, depending on food abundance, environmental temperatures, and other parameters, which leads to long-distance pathogen dispersion.

Despite these features that frequently bring bats in close contact with humans and agricultural animals, these mammals are very difficult to study. They are nocturnal, roost during the day high in tree canopies (such as pteropodid bats) or occupying small and narrow crevices in rocks, trees, buildings, or caves, and as such are frequently not readily available for direct observations, ecologic studies, and sampling. Not many bat species are tolerant to captivity, which would make them a reliable subject for laboratory experiments.

Nevertheless, as the attention to bats as infection reservoirs is increasing, more and more studies are being done which help to find pieces of the puzzle which, in time, will help us to understand the ecology of pathogen–bat interactions, their significance for veterinary and public health, and to develop appropriate prevention strategies which would protect humans and their animals, and at the same time, will not be severely harmful for bats themselves, as many of them are vulnerable to environmental changes, suffer from direct human interventions (e.g., hunting for food or extermination as an attempt to destroy disease reservoir, or simply “clean up” the dwellings occupied by bats due to the various inconveniences), and decline in numbers.

Studies of bat pathogens constitute several layers which partly overlap and complement each other. One layer consists of a random surveillance (usually performed as pilot pathogen discovery studies) which further usually focuses on specific hypotheses, is extended to longitudinal and latitudinal studies, frequently complemented with a modeling component. With certain flexibility, these efforts can be classified into the category of ecological studies of bat–pathogen interactions.

Another layer includes laboratory studies of bat–pathogen interactions. Part of these are done in vitro using bat cell lines (with very limited numbers by both, bat species and tissue types, available to date), which frequently requires the additional development of specific reagents that would react with bat proteins or nucleic acids. Another part is done in experimentally-infected bats, but only for a few pathogens is the relevant reservoir bat species known or can be successfully kept in captivity.

Further, a significant effort is dedicated to public health outreach, which includes surveys, analysis of the obtained data, and generation of strategies which would help to avoid bat exposure or implement prophylactic and treatment solutions if exposure occurs. An additional element frequently incorporated in such studies and based on the One Health concept is dedicated to bat protection—an ability to coexist near each other and not suffer from such a neighboring.

This Special Issue is dedicated to different studies of bat-borne pathogens that collectively contribute to better understanding of the existing complexities and outline further research and intervention strategies.

Dr. Ivan V. Kuzmin
Guest Editor

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Keywords

  • bats
  • chiroptera
  • bat
  • bat-borne
  • zoonosis
  • emerging infectious diseases
  • pathogens
  • virus
  • bacteria
  • One Health
  • immunity
  • protection

Published Papers (4 papers)

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Research

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11 pages, 1633 KiB  
Article
Paramyxo- and Coronaviruses in Rwandan Bats
by Wanda Markotter, Marike Geldenhuys, Petrus Jansen van Vuren, Alan Kemp, Marinda Mortlock, Antoine Mudakikwa, Louis Nel, Julius Nziza, Janusz Paweska and Jacqueline Weyer
Trop. Med. Infect. Dis. 2019, 4(3), 99; https://doi.org/10.3390/tropicalmed4030099 - 02 Jul 2019
Cited by 21 | Viewed by 8050
Abstract
A high diversity of corona- and paramyxoviruses have been detected in different bat species at study sites worldwide, including Africa, however no biosurveillance studies from Rwanda have been reported. In this study, samples from bats collected from caves in Ruhengeri, Rwanda, were tested [...] Read more.
A high diversity of corona- and paramyxoviruses have been detected in different bat species at study sites worldwide, including Africa, however no biosurveillance studies from Rwanda have been reported. In this study, samples from bats collected from caves in Ruhengeri, Rwanda, were tested for the presence of corona- and paramyxoviral RNA using reverse transcription PCR assays. Positive results were further characterized by DNA sequencing and phylogenetic analysis. In addition to morphological identification of bat species, we also did molecular confirmation of species identities, contributing to the known genetic database available for African bat species. We detected a novel Betacoronavirus in two Geoffroy’s horseshoe bats (Rhinolophus clivosus) bats. We also detected several different paramyxoviral species from various insectivorous bats. One of these viral species was found to be homologous to the genomes of viruses belonging to the Jeilongvirus genus. Additionally, a Henipavirus-related sequence was detected in an Egyptian rousette fruit bat (Rousettus aegyptiacus). These results expand on the known diversity of corona- and paramyxoviruses and their geographical distribution in Africa. Full article
(This article belongs to the Special Issue Emerging Tropical Pathogens of Bats)
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9 pages, 1708 KiB  
Article
Litomosoides sp. (Filarioidea: Onchocercidae) Infection in Frugivorous Bats (Artibeus spp.): Pathological Features, Molecular Evidence, and Prevalence
by Emilio Rendón-Franco, Osvaldo López-Díaz, Fernando Martínez-Hernández, Guiehdani Villalobos, Claudia Irais Muñoz-García, Nidia Aréchiga-Ceballos, Jorge Alberto Alfonso-Toledo, María Martha García Flores and Alvaro Aguilar Setién
Trop. Med. Infect. Dis. 2019, 4(2), 77; https://doi.org/10.3390/tropicalmed4020077 - 10 May 2019
Cited by 3 | Viewed by 3418
Abstract
Bats can host pathogenic organisms such as viruses and fungi, but little is known about the pathogenicity of their parasites. Hemoparasites are frequently recorded in Neotropical bats, particularly Litomosoides (Filarioidea: Onchocercidae), but their pathogenic effect on bats is scarcely known. In this work, [...] Read more.
Bats can host pathogenic organisms such as viruses and fungi, but little is known about the pathogenicity of their parasites. Hemoparasites are frequently recorded in Neotropical bats, particularly Litomosoides (Filarioidea: Onchocercidae), but their pathogenic effect on bats is scarcely known. In this work, Litomosoides microfilariae were identified in four (8%) out of 51 sampled frugivorous bats belonging to three different species: Artibeus aztecus, Artibeus jamaicensis, and Artibeus lituratus, which are located in Yautepec, Morelos, Mexico. Two infected animals showed weakness, tachypnoea, and ecchymosis on their wings. In these animals, histopathology revealed microfilariae in the blood vessels of the lung, liver, and spleen. Both animals presented exudative pneumonia with congestion and concomitant edema, in addition to moderate arterial hypertrophy. Parasitemia was quantified in blood samples of the infected animals (>3000 parasites/mL). Phylogenetic analysis placed the obtained sequence inside the Litomosoides genus, reaching over 98% identity to the related species. Due to the relevance of bats in ecosystems, any new record of their parasite repertoire offers noteworthy insights into our understanding of the ecology and impact of new parasite species in bats. Full article
(This article belongs to the Special Issue Emerging Tropical Pathogens of Bats)
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6 pages, 211 KiB  
Article
Assessment of a Rabies Virus Rapid Diagnostic Test for the Detection of Australian Bat Lyssavirus
by Andrea Certoma, Ross A. Lunt, Wilna Vosloo, Ina Smith, Axel Colling, David T. Williams, Thao Tran and Stuart D. Blacksell
Trop. Med. Infect. Dis. 2018, 3(4), 109; https://doi.org/10.3390/tropicalmed3040109 - 04 Oct 2018
Cited by 10 | Viewed by 3906
Abstract
Australian bat lyssavirus (ABLV) is closely related to the classical rabies virus and has been associated with three human fatalities and two equine fatalities in Australia. ABLV infection in humans causes encephalomyelitis, resulting in fatal disease, but has no effective therapy. The virus [...] Read more.
Australian bat lyssavirus (ABLV) is closely related to the classical rabies virus and has been associated with three human fatalities and two equine fatalities in Australia. ABLV infection in humans causes encephalomyelitis, resulting in fatal disease, but has no effective therapy. The virus is maintained in enzootic circulation within fruit bats (Pteropid spp.) and at least one insectivorous bat variety (Saccolaimus flaviventris). Most frequently, laboratory testing is conducted on pteropodid bat brains, either following a potential human exposure through bites, scratches and other direct contacts with bats, or as opportunistic assessment of sick or dead bats. The level of medical intervention and post-exposure prophylaxis is largely determined on laboratory testing for antigen/virus as the demonstrable infection status of the in-contact bat. This study evaluates the comparative diagnostic performance of a lateral flow test, Anigen Rabies Ag detection rapid test (RDT), in pteropodid variant of ABLV-infected bat brain tissues. The RDT demonstrated 100% agreement with the reference standard fluorescent antibody test on 43 clinical samples suggesting a potential application in rapid diagnosis of pteropodid variant of ABLV infection. A weighted Kappa value of 0.95 confirmed a high level of agreement between both tests. Full article
(This article belongs to the Special Issue Emerging Tropical Pathogens of Bats)

Review

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22 pages, 1423 KiB  
Review
Bats and Viruses: Emergence of Novel Lyssaviruses and Association of Bats with Viral Zoonoses in the EU
by Rebecca Shipley, Edward Wright, David Selden, Guanghui Wu, James Aegerter, Anthony R Fooks and Ashley C Banyard
Trop. Med. Infect. Dis. 2019, 4(1), 31; https://doi.org/10.3390/tropicalmed4010031 - 07 Feb 2019
Cited by 47 | Viewed by 10176
Abstract
Bats in the EU have been associated with several zoonotic viral pathogens of significance to both human and animal health. Virus discovery continues to expand the existing understating of virus classification, and the increased interest in bats globally as reservoirs or carriers of [...] Read more.
Bats in the EU have been associated with several zoonotic viral pathogens of significance to both human and animal health. Virus discovery continues to expand the existing understating of virus classification, and the increased interest in bats globally as reservoirs or carriers of zoonotic agents has fuelled the continued detection and characterisation of new lyssaviruses and other viral zoonoses. Although the transmission of lyssaviruses from bat species to humans or terrestrial species appears rare, interest in these viruses remains, through their ability to cause the invariably fatal encephalitis—rabies. The association of bats with other viral zoonoses is also of great interest. Much of the EU is free of terrestrial rabies, but several bat species harbor lyssaviruses that remain a risk to human and animal health. Whilst the rabies virus is the main cause of rabies globally, novel related viruses continue to be discovered, predominantly in bat populations, that are of interest purely through their classification within the lyssavirus genus alongside the rabies virus. Although the rabies virus is principally transmitted from the bite of infected dogs, these related lyssaviruses are primarily transmitted to humans and terrestrial carnivores by bats. Even though reports of zoonotic viruses from bats within the EU are rare, to protect human and animal health, it is important characterise novel bat viruses for several reasons, namely: (i) to investigate the mechanisms for the maintenance, potential routes of transmission, and resulting clinical signs, if any, in their natural hosts; (ii) to investigate the ability of existing vaccines, where available, to protect against these viruses; (iii) to evaluate the potential for spill over and onward transmission of viral pathogens in novel terrestrial hosts. This review is an update on the current situation regarding zoonotic virus discovery within bats in the EU, and provides details of potential future mechanisms to control the threat from these deadly pathogens. Full article
(This article belongs to the Special Issue Emerging Tropical Pathogens of Bats)
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