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

Deadline for manuscript submissions: closed (28 February 2023) | Viewed by 26316

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Prof. Dr. Anna Bajer

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Department of Eco-epidemiology of Parasitic Diseases, Institute of Developmental Biology and Biomedical Sciences, Faculty of Biology, University of Warsaw, Warsaw, Poland
Interests: parasitology; vector-borne diseases; tick-borne diseases; babesiosis; bartonellosis; dirofilariasis; vertical transmission of pathogens; protozoan diseases; cryptosporidiosis; giardiasis; rodent helminths; interactions in the parasite community; evolutionary history of parasites; genetic diversity; expansion of ticks/tick-borne diseases

Special Issue Information

Dear Colleagues,

Ticks are well-known vectors of a wide range of viral, bacterial, and protozoan pathogens in most regions of the world. In recent years, there has been a growing impact of tick-borne diseases on human and animal health. To control this trend, there is a need for an increase in the number of eco-epidemiological studies on ticks and tick-borne pathogens. In addition to well-studied tick species, such as Ixodes ricinus complex or Dermacentor reticulatus, more studies are needed on lesser known and reemerging tick species, as Haemaphysalis concinna or Hyalomma spp. Borreliosis (Lyme disease) is still among the most important tick-borne diseases, as it alone may affect a half million people annually in the Northern Hemisphere. Recognition of the factors influencing the occurrence of Lyme borreliosis is of high priority, together with a deepening of our knowledge on genetic diversity, pathogenesis, mechanisms of spirochete survival in tick vectors or possible interactions with the tick microbiome. Recently, the vertical route of transmission of tick-borne pathogens, form female to offspring, has also been explored in both environmental and laboratory studies.

In this Special Issue of Microorganisms, dedicated to ticks and tick-borne pathogens, we invite you to send your contributions concerning any aspects related to ticks and tick-borne pathogens, from the eco-epidemiological monitoring to the molecular phylogeny of novel species, and from basic to applied sciences.

Prof. Dr. Anna Bajer
Guest Editor

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Keywords

anaplasma phagocytophilum/anaplasmosis
babesia/babesiosis borrelia/borreliosis
co-infections
tick-borne diseases
tick-borne pathogens
tick-borne pathogen reservoir
tick-borne protozoa
tick-borne viruses
tick endosymbionts
tick expansion
tick microbiota

Published Papers (9 papers)

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Research

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10 pages, 616 KiB

Open AccessArticle

Preliminary Study on Artificial versus Animal-Based Feeding Systems for Amblyomma Ticks (Acari: Ixodidae)

by Patrick Stephan Sebastian, Nina Król, María Belén Novoa, Ard Menzo Nijhof, Martin Pfeffer, Santiago Nava and Anna Obiegala

Microorganisms 2023, 11(5), 1107; https://doi.org/10.3390/microorganisms11051107 - 24 Apr 2023

Cited by 2 | Viewed by 1510

Abstract

Hard ticks pose a threat to animal and human health. Active life stages need to feed on a vertebrate host in order to complete their life cycle. To study processes such as tick-pathogen interactions or drug efficacy and pharmacokinetics, it is necessary to maintain tick colonies under defined laboratory conditions, typically using laboratory animals. The aim of this study was to test a membrane-based artificial feeding system (AFS) applicable for Amblyomma ticks using Amblyomma tonelliae as a biological model. Adult ticks from a laboratory colony were fed in a membrane-based AFS. For comparison, other A. tonelliae adults were fed on calf and rabbit. The proportions of attached (AFS: 76%; calf/rabbit: 100%) and engorged females (AFS: 47.4%; calf/rabbit: 100%) in the AFS were significantly lower compared to animal-based feeding (p = 0.0265). The engorgement weight of in vitro fed ticks (

\bar{x}

= 658 mg; SD ± 259.80) did not significantly differ from that of ticks fed on animals (p = 0.3272, respectively 0.0947). The proportion of females that oviposited was 100% for all three feeding methods. However, the incubation period of eggs (

\bar{x}

= 54 days; SD ± 7) was longer in the AFS compared to conventional animal-based feeding (p = 0.0014);

\bar{x}

= 45 days; SD ± 2 in the rabbit and (p = 0.0144).

\bar{x}

= 48 days; SD ± 2 in the calf). Egg cluster hatching (

\bar{x}

= 41%; SD ± 44.82) was lower in the AFS than in the other feeding methods (rabbit:

\bar{x}

= 74%; SD ± 20; p = 0.0529; calf:

\bar{x}

= 81%; SD ± 22; p = 0.0256). Although the attachment, development, and the hatching of AFS ticks were below those from animal-based feeding, the method may be useful in future experiments. Nevertheless, further experiments with a higher number of tick specimens (including immature life stages) and different attractant stimuli are required to confirm the preliminary results of this study and to evaluate the applicability of AFS for Amblyomma ticks as an alternative to animal-based feeding methods. Full article

(This article belongs to the Special Issue Research on Ticks and Tick-Borne Pathogens)

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14 pages, 836 KiB

Open AccessArticle

The AxBioTick Study: Borrelia Species and Tick-Borne Encephalitis Virus in Ticks, and Clinical Responses in Tick-Bitten Individuals on the Aland Islands, Finland

by Nellie Carlströmer Berthén, Eszter Tompa, Susanne Olausson, Clara Nyberg, Dag Nyman, Malin Ringbom, Linda Perander, Joel Svärd, Per-Eric Lindgren, Pia Forsberg, Peter Wilhelmsson, Johanna Sjöwall and Marika Nordberg

Microorganisms 2023, 11(5), 1100; https://doi.org/10.3390/microorganisms11051100 - 22 Apr 2023

Viewed by 1741

Abstract

The AxBioTick study was initiated to investigate the prevalence of ticks and tick-borne pathogens and their impact on antibody and clinical responses in tick-bitten individuals on the Aland Islands. This geographical area is hyperendemic for both Lyme borreliosis (LB) and Tick-borne encephalitis (TBE). Blood samples and ticks were collected from 100 tick-bitten volunteers. A total of 425 ticks was collected, all determined to Ixodes ricinus using molecular tools. Of them 20% contained Borrelia species, of which B. garinii and B. afzelii were most common. None contained the TBE virus (TBEV). Blood samples were drawn in conjunction with the tick bite, and eight weeks later. Sera were analyzed for Borrelia- and TBEV-specific antibodies using an ELISA and a semiquantitative antibody assay. In total 14% seroconverted in Borrelia C6IgG1, 3% in TBEV IgG, and 2% in TBEV IgM. Five participants developed clinical manifestations of LB. The high seroprevalence of both Borrelia (57%) and TBEV (52%) antibodies are likely attributed to the endemic status of the corresponding infections as well as the TBE vaccination program. Despite the similar prevalence of Borrelia spp. detected in ticks in other parts of Europe, the infection rate in this population is high. The AxBioTick study is continuing to investigate more participants and ticks for co-infections, and to characterize the dermal immune response following a tick bite. Full article

(This article belongs to the Special Issue Research on Ticks and Tick-Borne Pathogens)

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12 pages, 2495 KiB

Open AccessArticle

Detection of Old and New World Relapsing Fever Borreliae in Ornithodoros Ticks Collected from Warthog Burrows in Zambia

by Yongjin Qiu, Herman M. Chambaro, Kozue Sato, David Squarre, Edgar Simulundu, Masahiro Kajihara, Katendi Changula, Manyando Simbotwe, Hayato Harima, Joseph Ndebe, Ladslav Moonga, Ryo Nakao, Ayato Takada, Bernard Mudenda Hang’ombe, Hirofumi Sawa and Hiroki Kawabata

Microorganisms 2023, 11(1), 200; https://doi.org/10.3390/microorganisms11010200 - 12 Jan 2023

Viewed by 2128

Abstract

Relapsing fever (RF) is an arthropod-borne disease caused by Borrelia spirochete, which is one of the major public health concerns in endemic regions including Africa. However, information on Borrelia spirochetes is limited in Zambia. Here, we investigate the Borrelia spirochetes harbored by Ornithodoros ticks in Zambian National Parks. We analyzed 182 DNA samples pooled from 886 Ornithodoros ticks. Of these, 43 tested positive, and their sequence revealed that the ticks harbored both Old and New World RF borreliae. This research presents the first evidence of Old-World RF borreliae in Zambia. The New World RF borreliae detected herein differed from the Candidatus Borrelia fainii previously reported in Zambia and were closely related to the pathogenic Borrelia sp. VS4 identified in Tanzania. Additionally, Borrelia theileri was recently reported in Zambia. Hence, at least four different Borrelia species occur in Zambia, and the organisms causing relapsing fever there might be more complex than previously thought. We empirically confirmed that real-time PCR with TaqMan minor groove binder probes accurately and simultaneously detected both Old and New World RF. In this manner, they could facilitate quantitative analyses of both types of RF borreliae. Subsequent investigations should endeavor to isolate the aforementioned Borrelia spp. and perform serosurveys on patients with RF. Full article

(This article belongs to the Special Issue Research on Ticks and Tick-Borne Pathogens)

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13 pages, 3086 KiB

Open AccessArticle

Hyalomma spp. in Austria—The Tick, the Climate, the Diseases and the Risk for Humans and Animals

by Georg Gerhard Duscher, Stefan Kienberger, Klaus Haslinger, Barbara Holzer, Irene Zimpernik, Reinhard Fuchs, Michael Schwarz, Peter Hufnagl, Peter Schiefer and Friedrich Schmoll

Microorganisms 2022, 10(9), 1761; https://doi.org/10.3390/microorganisms10091761 - 31 Aug 2022

Cited by 2 | Viewed by 1813

Abstract

Recently, ticks of Hyalomma spp. have been found more often in areas previously lacking this tick species. Due to their important role as a vector of different diseases, such as Crimean-Congo-hemorrhagic fever (CCHF), the occurrence and potential spread of this tick species is of major concern. So far, eight Hyalomma sp. ticks were found between 2018 and 2021 in Austria. A serological investigation on antibodies against the CCHF virus in 897 cattle as indicator animals displayed no positive case. During observation of climatic factors, especially in the period from April to September, the year 2018 displayed an extraordinary event in terms of higher temperature and dryness. To estimate the risk for humans to come in contact with Hyalomma sp. in Austria, many parameters have to be considered, such as the resting place of birds, availability of large livestock hosts, climate, density of human population, etc. Full article

(This article belongs to the Special Issue Research on Ticks and Tick-Borne Pathogens)

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18 pages, 775 KiB

Open AccessArticle

Co-Occurrence of Francisella, Spotted Fever Group Rickettsia, and Midichloria in Avian-Associated Hyalomma rufipes

by Tove Hoffman, Andreas Sjödin, Caroline Öhrman, Linda Karlsson, Ryelan Francis McDonough, Jason W. Sahl, Dawn Birdsell, David M. Wagner, Laura G. Carra, Peter Wilhelmsson, John H.-O. Pettersson, Christos Barboutis, Jordi Figuerola, Alejandro Onrubia, Yosef Kiat, Dario Piacentini, Thomas G. T. Jaenson, Per-Eric Lindgren, Sara Moutailler, Thord Fransson, Mats Forsman, Kenneth Nilsson, Åke Lundkvist and Björn Olsen Show full author list Hide full author list

Microorganisms 2022, 10(7), 1393; https://doi.org/10.3390/microorganisms10071393 - 11 Jul 2022

Cited by 3 | Viewed by 2313

Abstract

The migratory behavior of wild birds contributes to the geographical spread of ticks and their microorganisms. In this study, we aimed to investigate the dispersal and co-occurrence of Francisella and spotted fever group Rickettsia (SFGR) in ticks infesting birds migrating northward in the African-Western Palaearctic region (AWPR). Birds were trapped with mist nests across the Mediterranean basin during the 2014 and 2015 spring migration. In total, 575 ticks were collected from 244 birds. We screened the ticks for the species Francisella tularensis, the genus Francisella, and SFGR by microfluidic real-time PCR. Confirmatory analyses and metagenomic sequencing were performed on tick samples that putatively tested positive for F. tularensis during initial screenings. Hyalomma rufipes was the most common tick species and had a high prevalence of Francisella, including co-occurrence of Francisella and SFGR. Metagenomic analysis of total DNA extracted from two H. rufipes confirmed the presence of Francisella, Rickettsia, and Midichloria. Average nucleotide identity and phylogenetic inference indicated the highest identity of the metagenome-assembled genomes to a Francisella-like endosymbiont (FLE), Rickettsia aeschlimannii, and Midichloria mitochondrii. The results of this study suggest that (i) FLE- and SFGR-containing ticks are dispersed by northbound migratory birds in the AWPR, (ii) H. rufipes likely is not involved in transmission of F. tularensis in the AWPR, and (iii) a dual endosymbiosis of FLEs and Midichloria may support some of the nutritional requirements of H. rufipes. Full article

(This article belongs to the Special Issue Research on Ticks and Tick-Borne Pathogens)

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9 pages, 436 KiB

Open AccessCommunication

Comparison of DNA Extraction and Amplification Techniques for Use with Engorged Hard-Bodied Ticks

by Gretchen C. Reifenberger, Bryce A. Thomas and DeLacy V. L. Rhodes

Microorganisms 2022, 10(6), 1254; https://doi.org/10.3390/microorganisms10061254 - 20 Jun 2022

Cited by 5 | Viewed by 3759

Abstract

Tick-borne infections are a serious threat to humans, livestock, and companion animals in many parts of the world, often leading to high morbidity and mortality rates, along with decreased production values and/or costly treatments. The prevalence of the microbes responsible for these infections is typically assessed by the molecular identification of pathogens within the tick vectors. Ticks sampled from animals are often engorged with animal blood, presenting difficulties in the amplification of nucleic acids due to the inhibitory effects of mammalian blood on the enzymes used in polymerase chain reactions (PCRs). This study tested two tick preparation methods, three methods of DNA extraction, and four commercially available DNA polymerases to determine the most reliable method of extracting and amplifying DNA from engorged ticks. Our study found that the phenol–chloroform extraction method yielded the highest concentration of DNA, yet DNA extracted by this method was amplified the least successfully. Thermo Scientific’s Phusion Plus PCR Master Mix was the best at amplifying the tick 16s rRNA gene, regardless of extraction method. Finally, our study identified that using the Qiagen DNeasy Blood & Tissues kit for DNA extraction coupled with either Phusion Plus PCR Master Mix or GoTaq DNA polymerase Master Mix is the best combination for the optimized amplification of DNA extracted from engorged ticks. Full article

(This article belongs to the Special Issue Research on Ticks and Tick-Borne Pathogens)

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40 pages, 2080 KiB

Open AccessArticle

Distribution of Tick-Borne Pathogens in Domestic Animals and Their Ticks in the Countries of the Mediterranean Basin between 2000 and 2021: A Systematic Review

by Baptiste Defaye, Sara Moutailler, Vanina Pasqualini and Yann Quilichini

Microorganisms 2022, 10(6), 1236; https://doi.org/10.3390/microorganisms10061236 - 16 Jun 2022

Cited by 6 | Viewed by 3075

Abstract

Tick-borne pathogens (TBPs) include a wide range of bacteria, parasites and viruses that cause a large spectrum of animal, human and zoonotic tick-borne diseases (TBDs). The object of this review was to establish an inventory and an analysis of TBPs found in domestic animals in the countries of the Mediterranean Basin. This geographic area occupies a central position between several continents and is an area of movement for animals, humans and pathogens of interest and their vectors, which is important in terms of animal and human health. In this systematic review, we included a total of 271 publications produced between 2000–2021 concerning TBPs in domestic animals. Among this literature, we found a total of 90 pathogen species (known as TBPs) reported in the 20 countries of the area; these were detected in tick species from domestic animals and were also directly detected in domestic animals. In all, 31 tick species were recorded and 12 domestic animal species, the latter comprising nine livestock and three pet species. More than 50% of the publications were from Western Europe. Island data were extracted and assessed, as islands of the Mediterranean Basin were represented in 16% of the publications and 77.8% of the TBPs reported. Our results show the importance of islands in the monitoring of TBPs, despite the low percentage of publications. Full article

(This article belongs to the Special Issue Research on Ticks and Tick-Borne Pathogens)

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15 pages, 557 KiB

Open AccessArticle

Prevalence of Bacterial and Protozoan Pathogens in Ticks Collected from Birds in the Republic of Moldova

by Alexandr Morozov, Alexei Tischenkov, Cornelia Silaghi, Andrei Proka, Ion Toderas, Alexandru Movila, Hagen Frickmann and Sven Poppert

Microorganisms 2022, 10(6), 1111; https://doi.org/10.3390/microorganisms10061111 - 27 May 2022

Cited by 3 | Viewed by 2206

Abstract

Epidemiological knowledge on pathogens in ticks feeding on birds in Moldova is scarce. To reduce this gap of information, a total of 640 migrating and native birds of 40 species were caught from 2012 to 2015 and examined for the presence of ticks in the Republic of Moldova. Altogether, 262 ticks belonging to five tick species (Ixodes ricunus n = 245, Ixodes frontalis n = 12, Haemaphysalis punctata n = 2, Hyalomma marginatum n = 2 (only males), Dermacentor marginatus n = 1) were collected from 93 birds. Of these ticks, 250 (96%) were at the stage of a nymph and 9 at the stage of a larva (3%). One imago of I. frontalis and two imagoes of Hy. marginatum were found. Generally, ticks infested 14.1% of the assessed birds belonging to 12 species. DNA was extracted from individual ticks with subsequent PCR targeting Rickettsia spp., Borrelia spp. in general, as well as relapsing fever-associated Borrelia spp., in particular, Anaplasma phagocytophilum, Neoehrlichia mikurensis, Babesia spp. and Coxiella burnetii. The bird species Turdus merula showed the heaviest infestation with ticks and the highest incidence of infected ticks. Altogether, 32.8% of the assessed ticks (n = 86) were positive for one of the pathogens. DNA of Borrelia spp. was found in 15.2% (40/262) of the investigated ticks; in 7.6% of ticks (20/262), DNA of rickettsiae was detected; 6.9% (18/262) of the ticks were positive for A. phagocytophilum DNA; in 1.5% of the ticks (4/262), DNA of Neoehrlichia mikurensis was detected, followed by 1.5% (4/262) Babesia microti and 1.5% (4/262) Borrelia miyamotoi. Within the B. burgdorferi complex, B. garinii (n = 36) was largely predominant, followed by B. valaisiana (n = 2) and B. lusitaniae (n = 2). Among the detected Rickettsia spp., R. monacensis (n = 16), R. helvetica (n = 2) and R. slovaca (n = 1) were identified. In conclusion, the study provided some new information on the prevalence of ticks on birds in Moldova, as well as the presence of DNA of pathogens in the ticks. By doing so, it provided an additional piece in the puzzle of the global epidemiology of tick-transmitted infectious diseases from a geographic side from where respective surveillance data are scarce. Full article

(This article belongs to the Special Issue Research on Ticks and Tick-Borne Pathogens)

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Review

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39 pages, 1089 KiB

Open AccessReview

Babesiosis in Southeastern, Central and Northeastern Europe: An Emerging and Re-Emerging Tick-Borne Disease of Humans and Animals

by Anna Bajer, Ana Beck, Relja Beck, Jerzy M. Behnke, Dorota Dwużnik-Szarek, Ramon M. Eichenberger, Róbert Farkas, Hans-Peter Fuehrer, Mike Heddergott, Pikka Jokelainen, Michael Leschnik, Valentina Oborina, Algimantas Paulauskas, Jana Radzijevskaja, Renate Ranka, Manuela Schnyder, Andrea Springer, Christina Strube, Katarzyna Tolkacz and Julia Walochnik

Microorganisms 2022, 10(5), 945; https://doi.org/10.3390/microorganisms10050945 - 30 Apr 2022

Cited by 36 | Viewed by 5987

Abstract

There is now considerable evidence that in Europe, babesiosis is an emerging infectious disease, with some of the causative species spreading as a consequence of the increasing range of their tick vector hosts. In this review, we summarize both the historic records and recent findings on the occurrence and incidence of babesiosis in 20 European countries located in southeastern Europe (Bosnia and Herzegovina, Croatia, and Serbia), central Europe (Austria, the Czech Republic, Germany, Hungary, Luxembourg, Poland, Slovakia, Slovenia, and Switzerland), and northern and northeastern Europe (Lithuania, Latvia, Estonia, Iceland, Denmark, Finland, Sweden, and Norway), identified in humans and selected species of domesticated animals (cats, dogs, horses, and cattle). Recorded cases of human babesiosis are still rare, but their number is expected to rise in the coming years. This is because of the widespread and longer seasonal activity of Ixodes ricinus as a result of climate change and because of the more extensive use of better molecular diagnostic methods. Bovine babesiosis has a re-emerging potential because of the likely loss of herd immunity, while canine babesiosis is rapidly expanding in central and northeastern Europe, its occurrence correlating with the rapid, successful expansion of the ornate dog tick (Dermacentor reticulatus) populations in Europe. Taken together, our analysis of the available reports shows clear evidence of an increasing annual incidence of babesiosis across Europe in both humans and animals that is changing in line with similar increases in the incidence of other tick-borne diseases. This situation is of major concern, and we recommend more extensive and frequent, standardized monitoring using a “One Health” approach. Full article

(This article belongs to the Special Issue Research on Ticks and Tick-Borne Pathogens)

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