Vector-Borne Infections in Wildlife

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Veterinary Microbiology".

Deadline for manuscript submissions: closed (15 February 2024) | Viewed by 16452

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Guest Editor
Immunoparasitology Laboratory, Department of Pathology, Theriogenology, and One Health, School of Agricultural and Veterinary Sciences, São Paulo State University, UNESP, Jaboticabal 14884-900, SP, Brazil
Interests: vector-borne agents; wild animals; Bartonella; Hemoplasmas; Hepatozoon; Piroplasmida; Rickettsiales
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Special Issue Information

Dear Colleagues,

Recently, the incidence of vector-borne diseases in humans and animals has increased due to multiple factors, which in combination favor the chances of contact among wild animals and associated ectoparasites, domestic animals, and humans. The bi-directional flow of vector-borne pathogens may occur from wildlife to domestic animals and vice versa. The main factors associated with the emergence or re-emergence of vector-borne diseases are climate change (including global warming), “outdoor” activities, global traveling, urbanization, changes in land use, deforestation, habitat fragmentation, and natural environment encroachment. These factors together predispose to a higher contact among wildlife, humans, and domestic animals. At the same time, the use of molecular tools facilitates the diagnosis, identification, and genotyping of this group of pathogens. An increase in awareness of vector-borne agents/diseases by veterinarians, physicians, scientists, and public health authorities has resulted in the advance of knowledge on vector-borne infections in wild animals.

Wild animals are considered the primary source of vector-borne zoonotic agents to humans. The dynamic of vector-borne agent transmission has been driven by different vertebrate host species living in sympatry. In this scenario, the overlapping of different species’ ecological niches creates opportunities for these agents to spread their geographical distribution and host range and grow in numbers. As a consequence, several newly discovered arthropod-borne pathogens originating from wildlife have emerged or re-emerged.

This Special Issue of Microorganisms will include articles concerning vector-borne pathogens among different species of wild animals (free-ranging or captive), including those viewed under the ‘One Health’ approach. Submissions can refer to the causal agents of such infections, as well as to all aspects of relevant diseases: diagnosis, pathogenesis, transmission, epidemiology and molecular epidemiology, and surveillance and control. Studies performed in wild animals describing original field, laboratory or experimental work, as well as systematic or opinionated reviews are welcome.

Dr. Marcos Rogério André
Guest Editor

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Keywords

  • vector-borne agents
  • Bartonella, Borrelia
  • Haemosporida
  • Hemoplasmas
  • Hepatozoon
  • Filarids
  • Piroplasmida
  • Rickettsiales
  • Trypanosomatidae

Published Papers (8 papers)

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Research

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16 pages, 2833 KiB  
Article
Molecular Investigation Confirms Myotis Genus Bats as Common Hosts of Polychromophilus in Brazil
by Bruno da Silva Mathias, Guilherme Augusto Minozzo, Alexander Welker Biondo, Jaciara de Oliveira Jorge Costa, Herbert Sousa Soares, Arlei Marcili, Lilian de Oliveira Guimarães, Carolina Clares dos Anjos, Andrea Pires Dos Santos, Irina Nastassja Riediger, Alan Fecchio, Marina Galvão Bueno, João Batista Pinho and Karin Kirchgatter
Microorganisms 2023, 11(6), 1531; https://doi.org/10.3390/microorganisms11061531 - 08 Jun 2023
Cited by 1 | Viewed by 1590
Abstract
Plasmodium spp. and some other blood parasites belonging to the order Haemosporida are the focus of many epidemiological studies worldwide. However, haemosporidian parasites from wild animals are largely neglected in scientific research. For example, Polychromophilus parasites, which are exclusive to bats, are described [...] Read more.
Plasmodium spp. and some other blood parasites belonging to the order Haemosporida are the focus of many epidemiological studies worldwide. However, haemosporidian parasites from wild animals are largely neglected in scientific research. For example, Polychromophilus parasites, which are exclusive to bats, are described in Europe, Asia, Africa, and Oceania, but little is known about their presence and genetic diversity in the New World. In this study, 224 samples of bats from remaining fragments of the Atlantic Forest and Pantanal biomes, as well as urbanized areas in southern and southeastern Brazil, were analyzed for the presence of haemosporidian parasites by PCR of the mitochondrial gene that encodes cytochrome b (cytb). The PCR fragments of the positive samples were sequenced and analyzed by the Bayesian inference method to reconstruct the phylogenetic relationships between Polychromophilus parasites from bats in Brazil and other countries. Sequences from Brazilian lineages of Polychromophilus were recovered in a clade with sequences from Polychromophilus murinus and close to the one Polychromophilus sequence obtained in Panama, the only available sequence for the American continent. This clade was restricted to bats of the family Vespertilionidae and distinct from Polychromophilus melanipherus, a parasite species mainly found in bats of the family Miniopteridae. The detection of Polychromophilus and the genetic proximity to P. murinus were further confirmed with the amplification of two other genes (clpc and asl). We also found a Haemosporida parasite sequence in a sample of Noctilio albiventris collected in the Pantanal biome, which presents phylogenetic proximity with avian Haemoproteus sequences. Morphological and molecular studies are still needed to conclude and describe the Polychromophilus species in Brazilian Myotis bats in more detail and to confirm Haemoproteus parasites in bats. Nevertheless, these molecular results in Brazilian bats confirm the importance of studying these neglected genera. Full article
(This article belongs to the Special Issue Vector-Borne Infections in Wildlife)
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10 pages, 965 KiB  
Article
Occurrence of Leishmaniasis in Iberian Wolves in Northwestern Spain
by Javier Merino Goyenechea, Verónica Castilla Gómez de Agüero, Jesús Palacios Alberti, Rafael Balaña Fouce and María Martínez Valladares
Microorganisms 2023, 11(5), 1179; https://doi.org/10.3390/microorganisms11051179 - 30 Apr 2023
Viewed by 2050
Abstract
Canine leishmaniasis is an important vector-borne protozoan disease in dogs that is responsible for serious deterioration in their health. In the Iberian Peninsula, as in most countries surrounding the Mediterranean Sea, canine leishmaniasis is caused by Leishmania infantum (zymodeme MON-1), a digenetic trypanosomatid [...] Read more.
Canine leishmaniasis is an important vector-borne protozoan disease in dogs that is responsible for serious deterioration in their health. In the Iberian Peninsula, as in most countries surrounding the Mediterranean Sea, canine leishmaniasis is caused by Leishmania infantum (zymodeme MON-1), a digenetic trypanosomatid that harbors in the parasitophorous vacuoles of host macrophages, causing severe lesions that can lead to death if the animals do not receive adequate treatment. Canine leishmaniasis is highly prevalent in Spain, especially in the Mediterranean coastal regions (Levante, Andalusia and the Balearic Islands), where the population of domestic dogs is very high. However, the presence of this disease has been spreading to other rural and sparsely populated latitudes, and cases of leishmaniasis have been reported for years in wildlife in northwestern Spain. This work describes for the first time the presence of wolves that tested positive for leishmaniasis in the vicinity of the Sierra de la Culebra (Zamora province, northwestern Spain), a protected sanctuary of this canid species, using PCR amplification of L. infantum DNA from different non-invasive samples such as buccal mucosa and those from both ears and hair. In addition to live animals (21), samples from carcasses of mainly roadkill animals (18) were also included and analyzed using the same technique, obtaining a positivity rate of 18 of the 39 wolves sampled (46.1%) regardless of their origin. Full article
(This article belongs to the Special Issue Vector-Borne Infections in Wildlife)
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25 pages, 5637 KiB  
Article
Understanding Habitats and Environmental Conditions of White-Tailed Deer Population Density and Public Health Data to Aid in Assessing Human Tick-Borne Disease Risk
by Sarah P. Maxwell, Chris Brooks, Pyung Kim, Dohyeong Kim, Connie L. McNeely and Kevin Thomas
Microorganisms 2023, 11(4), 865; https://doi.org/10.3390/microorganisms11040865 - 28 Mar 2023
Cited by 2 | Viewed by 2361
Abstract
The extent of tick-borne diseases (TBDs) in the United States is largely unknown and underreported. Equitable diagnostic and treatment options may vary by geographic location. Triangulating multi-modal data sources informed by a One Health approach provides robust proxies for human TBD risk. Using [...] Read more.
The extent of tick-borne diseases (TBDs) in the United States is largely unknown and underreported. Equitable diagnostic and treatment options may vary by geographic location. Triangulating multi-modal data sources informed by a One Health approach provides robust proxies for human TBD risk. Using data from the Indiana Department of Natural Resources collected from hunters during the white-tailed deer (Odocoileus virginianus) hunting season and other sources, we employ a mixed-methods approach based on thematic mapping and mixed effects modelling to determine if deer population density aligns with official disease data at the county level from (1) positive canine serological reports for, anaplasmosis, and Lyme Disease (LD); (2) positive human cases of ehrlichiosis, anaplasmosis, LD, and Spotted Fever rickettsioses; and (3) tick infectivity. We propose the need for multimodal data analysis using a variety of potential proxies to better estimate disease risk and inform public health policy and practice. We find similar spatial distributions between deer population density and human and canine TBDs in northeastern and southern Indiana, which are rural and mixed geographic areas. Overall, LD is more prevalent in the northwest, central-western, and southeastern counties, while ehrlichiosis is more common in the southern counties. These findings hold true across humans, canines, and deer. Full article
(This article belongs to the Special Issue Vector-Borne Infections in Wildlife)
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15 pages, 6557 KiB  
Article
Multi-Locus Sequencing Reveals Putative Novel Anaplasmataceae Agents, ‘Candidatus Ehrlichia dumleri’ and Anaplasma sp., in Ring-Tailed Coatis (Carnivora: Nasua nasua) from Urban Forested Fragments at Midwestern Brazil
by Lívia Perles, Heitor M. Herrera, Wanessa T. G. Barreto, Gabriel C. de Macedo, Ana C. Calchi, Rosangela Z. Machado and Marcos R. André
Microorganisms 2022, 10(12), 2379; https://doi.org/10.3390/microorganisms10122379 - 30 Nov 2022
Cited by 4 | Viewed by 1403
Abstract
The Anaplasmataceae family encompasses obligate intracellular α-proteobacteria of human and veterinary medicine importance. This study performed multi-locus sequencing to characterize Ehrlichia and Anaplasma in coati’s blood samples in Midwestern Brazil. Twenty-five samples (25/165—15.1%) were positive in the screening PCR based on the dsb [...] Read more.
The Anaplasmataceae family encompasses obligate intracellular α-proteobacteria of human and veterinary medicine importance. This study performed multi-locus sequencing to characterize Ehrlichia and Anaplasma in coati’s blood samples in Midwestern Brazil. Twenty-five samples (25/165—15.1%) were positive in the screening PCR based on the dsb gene of Ehrlichia spp. and were characterized using 16S rRNA, sodB, groEL, and gltA genes and the 23S-5S intergenic space region (ITS). Phylogenetic analyses based on all six molecular markers positioned the sequences into a new clade, with a common origin of Ehrlichia ruminantium. Haplotype analyses of 16S RNA sequences revealed the presence of two distinct Ehrlichia genotypes. Six samples (6/165, 3.6%) were positive in the screening nPCR for the 16S rRNA gene of Anaplasma spp. and were submitted to an additional PCR targeting the ITS for molecular characterization. Phylogenetic analyses based on both 16S rRNA gene and ITS positioned the Anaplasma sp. detected in the present study in a large clade with other Anaplasma sp. previously detected in ticks and wild animals and in a clade with ‘Candidatus Anaplasma brasiliensis’, respectively. Based on distinct molecular markers, the present work described a putative novel Anaplasmataceae agent, namely ‘Candidatus Ehrlichia dumleri’, and Anaplasma sp. closely related to the previously described ‘Candidatus Anaplasma brasiliensis’. Full article
(This article belongs to the Special Issue Vector-Borne Infections in Wildlife)
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15 pages, 3672 KiB  
Article
Theileria terrestris nov. sp.: A Novel Theileria in Lowland Tapirs (Tapirus terrestris) from Two Different Biomes in Brazil
by Anna Claudia Baumel Mongruel, Emília Patrícia Medici, Ariel da Costa Canena, Ana Cláudia Calchi, Lívia Perles, Bianca Cardenal Balla Rodrigues, João Fabio Soares, Rosangela Zacarias Machado and Marcos Rogério André
Microorganisms 2022, 10(12), 2319; https://doi.org/10.3390/microorganisms10122319 - 23 Nov 2022
Cited by 4 | Viewed by 1633
Abstract
The low-land tapir (Tapirus terrestris) is the largest wild terrestrial mammal found in Brazil. Although T. terrestris has been already reported as a host of hemoparasites, the occurrence and genetic identity of Piroplasmida agents in this species is still cloudy. Although [...] Read more.
The low-land tapir (Tapirus terrestris) is the largest wild terrestrial mammal found in Brazil. Although T. terrestris has been already reported as a host of hemoparasites, the occurrence and genetic identity of Piroplasmida agents in this species is still cloudy. Although it is reported that Theileria equi, an endemic equid-infective agent in Brazil, is occurring in lowland tapirs, these reports are probably misconceived diagnoses since they are solely based on small fragments of 18S rRNA that may not achieve accurate topologies on phylogenetic analyses. The present study aimed to detect and investigate the identity of Theileria spp. in tapirs from Pantanal and Cerrado biomes. Blood-DNA samples from tapirs were screened for a partial (~800 bp) 18S rRNA gene fragment from Piroplasmida and 64 (64/122; 52.46% CI: 43.66–61.11%) presented bands of expected size. Samples were submitted to different protocols for molecular characterization, including near-full length 18S rRNA gene (~1500 bp), and the ema-1 gene from T. equi. Eight sequences were obtained for extended fragments (1182–1473 bp) from the 18S rRNA gene. Moreover, three sequences from partial cox-1 and five from partial hsp70 gene were obtained. None of the samples presented amplifications for the ema-1 gene. Phylogenetic and distance analyses from the 18S rRNA sequences obtained demonstrated a clear separation from tapirs’ Theileria spp. and T. equi. Phylogenetic analyses of cox-1 and hsp70 sequences obtained herein also showed a unique clade formed by tapir’s Theileria spp. Theileria terrestris sp. nov. is positioned apart from all other Theileria species in 18S rRNA, cox-1, and hps70 phylogenetic analyses. This novel proposed species represents a new Piroplasmida clade, yet to be characterized regarding biological features, vectors involved in the transmission cycles, additional vertebrate hosts, and pathogenicity. Full article
(This article belongs to the Special Issue Vector-Borne Infections in Wildlife)
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15 pages, 2552 KiB  
Article
Candidatus Mycoplasma Haemoalbiventris’ and Tick-Borne Pathogens in Black-Eared Opossum (Didelphis aurita) from Southeastern Brazil
by Andrés Maurício Ortega Orozco, Lucas Drumond Bento, Pollyanna Cordeiro Souto, Fabricia Modolo Girardi, Bárbara Cristina Félix Nogueira, Ricardo Seiti Yamatogi, Artur Kanadani Campos, Carolyn Cray, Fabiano Montiani-Ferreira, Flávia Carolina Meira Collere, Thállitha Samih Wischral Jayme Vieira, Rafael Felipe da Costa Vieira and Leandro Abreu da Fonseca
Microorganisms 2022, 10(10), 1955; https://doi.org/10.3390/microorganisms10101955 - 30 Sep 2022
Cited by 2 | Viewed by 1810
Abstract
The black-eared opossum (Didelphis aurita) is a South American synanthropic marsupial. The presence of opossums in domestic spaces is relevant in the One-Health context since they are hosts of pathogens and ectoparasites that may affect the health of domestic animals and [...] Read more.
The black-eared opossum (Didelphis aurita) is a South American synanthropic marsupial. The presence of opossums in domestic spaces is relevant in the One-Health context since they are hosts of pathogens and ectoparasites that may affect the health of domestic animals and humans. In this study, we aim to determine the occurrence of hemoplasmas and selected tick-borne pathogens in free-ranging black-eared opossums, along with their molecular characterization, hematological and biochemical evaluation and factors associated with infection, in the municipality of Viçosa, State of Minas Gerais, southeastern Brazil. Thirty black-eared opossums were trapped between March 2021 and June 2022. Ectoparasites were collected. Hematological and biochemical analyses were performed. DNA from EDTA-blood samples were analyzed by PCR and qPCR assays. By molecular analyses, ‘Candidatus Mycoplasma haemoalbiventris’ was the most prevalent hemoparasite (73.3%), followed by Hepatozoon sp. (22.2%). Significant differences were observed in the number of platelets, and in the concentration of protein and globulins in the animals infected by ‘Ca. M. haemoalbiventris’ when compared with the negative group. This is the first report of ‘Ca. M. haemoalbiventris’ infection in D. aurita. Full article
(This article belongs to the Special Issue Vector-Borne Infections in Wildlife)
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22 pages, 10296 KiB  
Article
First Report of Bartonella spp. in Marsupials from Brazil, with a Description of Bartonella harrusi sp. nov. and a New Proposal for the Taxonomic Reclassification of Species of the Genus Bartonella
by Renan Bressianini do Amaral, Marita Vedovelli Cardozo, Alessandro de Mello Varani, Maria Eduarda Chiaradia Furquim, Clara Morato Dias, William Oliveira de Assis, Alanderson Rodrigues da Silva, Heitor Miraglia Herrera, Rosangela Zacarias Machado and Marcos Rogério André
Microorganisms 2022, 10(8), 1609; https://doi.org/10.3390/microorganisms10081609 - 09 Aug 2022
Cited by 12 | Viewed by 2036
Abstract
The genus Bartonella (Rhizobiales: Bartonellaceae) encompasses facultative intracellular Gram-negative alphaproteobacteria that parasitize mainly erythrocytes and endothelial cells, as well as macrophages, monocytes and dendritic cells. Although they can infect numerous mammal species and arthropod vectors worldwide, reports of Bartonella infections in marsupials are [...] Read more.
The genus Bartonella (Rhizobiales: Bartonellaceae) encompasses facultative intracellular Gram-negative alphaproteobacteria that parasitize mainly erythrocytes and endothelial cells, as well as macrophages, monocytes and dendritic cells. Although they can infect numerous mammal species and arthropod vectors worldwide, reports of Bartonella infections in marsupials are scarce. In fact, such agents have only been detected in marsupials and/or associated ectoparasites in Australia and the United States of America until the present moment. The present study aimed to isolate and characterize molecularly, morphologically and phenotypically Bartonella infecting free-living marsupials sampled in the Brazilian Pantanal, the largest wetland in South America. Two marsupials were captured in December 2018 and six marsupials in February 2019, totaling eight small mammals sampled: five (62.5%) Thylamys macrurus and three (37.5%) Monodelphis domestica. All blood samples were submitted to qPCR for Bartonella spp. based on the nuoG gene, a pre-enrichment liquid culture and a chocolate agar solid culture. Bartonella sp. was isolated from 3 T. macrurus and one M. domestica. One Bartonella isolate obtained from a T. macrurus blood sample (strain 117A) that showed to be closely related to the Bartonella vinsonii complex and Bartonella machadoae was selected for whole genome sequencing using a hybrid approach based on Illumina NovaSeq and Nanopore sequencing platforms. This strain showed a genome of 2.35 Mbp, with an average C + G content of 38.8%, coding for 2013 genes, and a 29 kb plasmid with an average C + G content of 34.5%. In addition, this strain exhibited an average nucleotide identity (ANI) of 85% with Bartonella species belonging to the B. vinsonii group and 91% with B. machadoae. Phylogenomic analysis based on 291 protein coding genes shared by the genomes of 53 Bartonella species positioned this strain closely to B. machadoae. This new isolated species was named Bartonella harrusi sp. nov., which was characterized as having small capnophilic, microaerophilic and aerobic rods with an absence of pili and flagella. In conclusion, the present work describes the biochemical, phenotypic and genomic characteristics of Bartonella harrusi, a new species isolated from the T. macrurus blood samples of the Brazilian Pantanal. Finally, a review of the taxonomic classification of members of the genus Bartonella is proposed, based on the ANI values accessed by whole genome sequencing analyses. Full article
(This article belongs to the Special Issue Vector-Borne Infections in Wildlife)
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Review

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31 pages, 1391 KiB  
Review
A Systematic Review of the Distribution of Tick-Borne Pathogens in Wild Animals and Their Ticks in the Mediterranean Rim between 2000 and 2021
by Baptiste Defaye, Sara Moutailler, Vanina Pasqualini and Yann Quilichini
Microorganisms 2022, 10(9), 1858; https://doi.org/10.3390/microorganisms10091858 - 16 Sep 2022
Viewed by 2266
Abstract
Tick-borne pathogens (TBPs) can be divided into three groups: bacteria, parasites, and viruses. They are transmitted by a wide range of tick species and cause a variety of human, animal, and zoonotic diseases. A total of 148 publications were found on tick-borne pathogens [...] Read more.
Tick-borne pathogens (TBPs) can be divided into three groups: bacteria, parasites, and viruses. They are transmitted by a wide range of tick species and cause a variety of human, animal, and zoonotic diseases. A total of 148 publications were found on tick-borne pathogens in wild animals, reporting on 85 species of pathogens from 35 tick species and 17 wild animal hosts between 2000 and February 2021. The main TBPs reported were of bacterial origin, including Anaplasma spp. and Rickettsia spp. A total of 72.2% of the TBPs came from infected ticks collected from wild animals. The main tick genus positive for TBPs was Ixodes. This genus was mainly reported in Western Europe, which was the focus of most of the publications (66.9%). It was followed by the Hyalomma genus, which was mainly reported in other areas of the Mediterranean Rim. These TBPs and TBP-positive tick genera were reported to have come from a total of 17 wild animal hosts. The main hosts reported were game mammals such as red deer and wild boars, but small vertebrates such as birds and rodents were also found to be infected. Of the 148 publications, 12.8% investigated publications on Mediterranean islands, and 36.8% of all the TBPs were reported in seven tick genera and 11 wild animal hosts there. The main TBP-positive wild animals and tick genera reported on these islands were birds and Hyalomma spp. Despite the small percentage of publications focusing on ticks, they reveal the importance of islands when monitoring TBPs in wild animals. This is especially true for wild birds, which may disseminate their ticks and TBPs along their migration path. Full article
(This article belongs to the Special Issue Vector-Borne Infections in Wildlife)
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