Advances in Tick Research

A topical collection in Pathogens (ISSN 2076-0817). This collection belongs to the section "Ticks".

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Editors

UMR BIPAR, INRAE, ANSES, Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, 94700 Maisons-Alfort, France
Interests: tick-host-pathogen interactions; emerging tick-borne pathogens; Anaplasma; Ehrlichia; epidemiology; tick microbiome; α-Gal
Special Issues, Collections and Topics in MDPI journals
UMR BIPAR, INRA, ANSES, Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, 94700 Maisons-Alfort, France
Interests: tick neuro-physiology; signal transductions; neuropeptides; neurotransmitters; GPCRs
Special Issues, Collections and Topics in MDPI journals
Institute of Parasitology, Biology Centre, Czech Academy of Sciences, Branišovska 1160/31, CZ-37005, České Budějovice, Czech Republic
Veterinary Research Institute, Hudcova 70, CZ-62100, Brno, Czech Republic
Interests: Thermodynamics of drug therapy against vector-based diseases
School of Environmental Sciences, University of Guelph, N1G 2W1, ON, Canada
Interests: Preventive veterinary medicine; microbial ecology; vector-borne pathogens; host-pathogen interaction; functional metagenomics
Special Issues, Collections and Topics in MDPI journals

Topical Collection Information

Dear Colleagues,

Ticks, along with mites, are arachnids that constitute the subclass Acari. Molecular clock estimates that ticks originated in the Carboniferous era, approximately 300 million years ago. Fossil records also support that ticks were blood-suckers of dinosaurs 100 million years ago. The unusual adaptation of tick physiology that directly reflects the challenges of their fluctuating environment is incomparable to any other blood feeding arthropod. The pharmacopeia of tick salivary proteins is an arsenal for ticks to counteract host defense mechanisms. Although tick salivary proteins belong to known structural families, the function of these salivary proteins has diversified throughout tick evolution. Besides causing direct damage associated with blood feeding, and in some cases toxicity, ticks transmit a wide variety of pathogens, including bacteria, viruses, protozoa, and helminths. New genetic variants of these pathogens frequently emerge with an unforeseen impact on human and animal health. In addition to pathogens, ticks harbor some complex microbial communities that influence tick-pathogen interactions and potentially tick physiology. Currently, tick control overuse acaricides with substantial drawbacks that include environmental damage, human poisonings and the emergence of multiacaricide-resistant ticks. Anti-tick vaccines are an alternative for the control of one-host ticks (e.g., Rhipicephalus microplus). Implementing vaccination, however, has significant limitations - specifically against ticks that fed on multiple hosts during their life cycle. The aim of this Topical Collection, ‘New Frontiers in Tick Research’, is to explore the research landscape to find novel developments that may impact tick biology, tick-borne pathogen epidemiology, and strategies for controlling ticks and tick-borne pathogens.

Dr. Alejandro Cabezas-Cruz
Dr. Ladislav Šimo
Dr. James J. Valdés
Dr. Dasiel Obregón
Collection Editors

Manuscript Submission Information

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Keywords

  • Vector physiology
  • Structural biology of vector/viral proteins
  • Functional vector metagenomics
  • Factors shaping the structure of vector microbiome
  • Emerging vector-borne pathogens
  • Vector-host-pathogen interactions
  • Challenges in vector-borne pathogen detection
  • Drug discovery in vector-borne pathogens
  • Biocontrol of vectors
  • Advanced tools in vector researh

Published Papers (28 papers)

2023

Jump to: 2022, 2021, 2020

12 pages, 1359 KiB  
Article
Efficacy of the Vaccine Candidate Based on the P0 Peptide against Dermacentor nitens and Ixodes ricinus Ticks
by Alina Rodríguez-Mallon, Pedro E. Encinosa Guzmán, Yamil Bello, Ana Domingos, Sandra Antunes, Petr Kopacek, Ana Sofia Santos, Rita Velez, Jan Perner, Frank L. Ledesma Bravo, Helena Frantova, Jan Erhart, Rafmary Rodríguez, Alier Fuentes, David Diago, Marisdania Joglar, Luis Méndez and Mario Pablo Estrada
Pathogens 2023, 12(11), 1365; https://doi.org/10.3390/pathogens12111365 - 17 Nov 2023
Cited by 1 | Viewed by 1060
Abstract
The control of ticks through vaccination offers a sustainable alternative to the use of chemicals that cause contamination and the selection of resistant tick strains. However, only a limited number of anti-tick vaccines have reached commercial realization. In this sense, an antigen effective [...] Read more.
The control of ticks through vaccination offers a sustainable alternative to the use of chemicals that cause contamination and the selection of resistant tick strains. However, only a limited number of anti-tick vaccines have reached commercial realization. In this sense, an antigen effective against different tick species is a desirable target for developing such vaccines. A peptide derived from the tick P0 protein (pP0) conjugated to a carrier protein has been demonstrated to be effective against the Rhipicephalus microplus, Rhipicephalus sanguineus, and Amblyomma mixtum tick species. The aim of this work was to assess the efficacy of this peptide when conjugated to the Bm86 protein against Dermacentor nitens and Ixodes ricinus ticks. An RNAi experiment using P0 dsRNA from I. ricinus showed a dramatic reduction in the feeding of injected female ticks on guinea pigs. In the follow-up vaccination experiments, rabbits were immunized with the pP0-Bm86 conjugate and challenged simultaneously with larvae, nymphs, and the adults of I. ricinus ticks. In the same way, horses were immunized with the pP0-Bm86 conjugate and challenged with D. nitens larva. The pP0-Bm86 conjugate showed efficacies of 63% and 55% against I. ricinus and D. nitens ticks, respectively. These results, combined with previous reports of efficacy for this conjugate, show the promising potential for its development as a broad-spectrum anti-tick vaccine. Full article
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12 pages, 1676 KiB  
Article
Susceptibility of Amblyomma sculptum, Vector of Rickettsia rickettsii, Ticks from a National Park and an Experimental Farm to Different Synthetic Acaricides
by Ennya Rafaella Neves Cardoso, Stephani Félix Carvalho, Sarah Alves Dias, Rayane Almeida Santos, Mariana Avelar Tavares, Lucianne Cardoso Neves, Warley Vieira de Freitas Paula, Gracielle Teles Pádua, Nicolas Jalowitzki de Lima, Raquel Loren dos Reis Paludo, Isabela Santos Silva, Raphaela Bueno Mendes Bittencourt, Gabriel Cândido dos Santos, Flavia Giovana de Jesus Nascimento, Luiza Gabriella Ferreira de Paula, Filipe Dantas-Torres, Caio Marcio De Oliveira Monteiro and Felipe da Silva Krawczak
Pathogens 2023, 12(11), 1304; https://doi.org/10.3390/pathogens12111304 - 31 Oct 2023
Viewed by 827
Abstract
Amblyomma sculptum is a relevant tick species from a One Health perspective, playing an important role as a vector of Rickettsia rickettsii, the main agent of spotted fever rickettsiosis in Brazil. In this study, we evaluated the susceptibility of two A. sculptum [...] Read more.
Amblyomma sculptum is a relevant tick species from a One Health perspective, playing an important role as a vector of Rickettsia rickettsii, the main agent of spotted fever rickettsiosis in Brazil. In this study, we evaluated the susceptibility of two A. sculptum populations from Goiás state (midwestern Brazil) to different acaricides. The first tick population (GYN strain) originated from an experimental farm, where the ticks are annually exposed to acaricides. The second (PNE strain) was collected in a national park (Emas National Park), where the ticks had not been exposed to acaricides. Immersion tests were conducted with 21-day-old laboratory-reared larvae and nymphs originating from adult ticks collected in the areas mentioned above. The chosen acaricides were two synthetic pyrethroids (cypermethrin and deltamethrin), one organophosphate (chlorfenvinphos), one formamidine (amitraz), and two combinations of pyrethroids and organophosphates (cypermethrin, chlorpyrifos and citronellal; cypermethrin, fenthion and chlorpyrifos). Mortality data were used to determine the lethal concentration (LC) values at which 50%, 90%, and 99% of the ticks died (LC50, LC90, and LC99, respectively), and resistance ratios (RR) were calculated based on the LC values. The RR revealed differences between the acaricide-exposed (GYN) and unexposed (PNE) tick strains. The PNE strain larvae and nymphs were susceptible to all the tested acaricides. The GYN strain larvae were tolerant to cypermethrin, whereas the nymphs were tolerant to deltamethrin, chlorfenvinphos, and the combination of cypermethrin, chlorpyrifos, and citronellal (2 < RR ≤ 10). The GYN strain nymphs were resistant to amitraz (RR > 10). This is the first report of A. sculptum nymphs with resistance to amitraz and tolerance to deltamethrin, chlorfenvinphos, and the combination of cypermethrin, chlorpyrifos, and citronellal. Full article
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18 pages, 2264 KiB  
Review
Rabbits as Animal Models for Anti-Tick Vaccine Development: A Global Scenario
by Arlex Rodríguez-Durán, Shafi Ullah, Luís Fernando Parizi, Abid Ali and Itabajara da Silva Vaz Junior
Pathogens 2023, 12(9), 1117; https://doi.org/10.3390/pathogens12091117 - 01 Sep 2023
Cited by 2 | Viewed by 1294
Abstract
Studies evaluating candidate tick-derived proteins as anti-tick vaccines in natural hosts have been limited due to high costs. To overcome this problem, animal models are used in immunization tests. The aim of this article was to review the use of rabbits as an [...] Read more.
Studies evaluating candidate tick-derived proteins as anti-tick vaccines in natural hosts have been limited due to high costs. To overcome this problem, animal models are used in immunization tests. The aim of this article was to review the use of rabbits as an experimental model for the evaluation of tick-derived proteins as vaccines. A total of 57 tick proteins were tested for their immunogenic potential using rabbits as models for vaccination. The most commonly used rabbit breeds were New Zealand (73.8%), Japanese white (19%), Californians (4.8%) and Flemish lop-eared (2.4%) rabbits. Anti-tick vaccines efficacy resulted in up to 99.9%. Haemaphysalis longicornis (17.9%) and Ornithodoros moubata (12.8%) were the most common tick models in vaccination trials. Experiments with rabbits have revealed that some proteins (CoAQP, OeAQP, OeAQP1, Bm86, GST-Hl, 64TRP, serpins and voraxin) can induce immune responses against various tick species. In addition, in some cases it was possible to determine that the vaccine efficacy in rabbits was similar to that of experiments performed on natural hosts (e.g., Bm86, IrFER2, RmFER2, serpins and serine protease inhibitor). In conclusion, results showed that prior to performing anti-tick vaccination trials using natural hosts, rabbits can be used as suitable experimental models for these studies. Full article
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14 pages, 1528 KiB  
Article
Dynamics of Infections in Cattle and Rhipicephalus microplus: A Preliminary Study
by Elianne Piloto-Sardiñas, Angélique Foucault-Simonin, Alejandra Wu-Chuang, Lourdes Mateos-Hernández, Roxana Marrero-Perera, Lianet Abuin-Denis, Lisset Roblejo-Arias, Cristian Díaz-Corona, Zbigniew Zając, Joanna Kulisz, Aneta Woźniak, Sara Moutailler, Belkis Corona-González and Alejandro Cabezas-Cruz
Pathogens 2023, 12(8), 998; https://doi.org/10.3390/pathogens12080998 - 30 Jul 2023
Cited by 1 | Viewed by 1182
Abstract
Tick-borne pathogens (TBPs) pose a significant threat to livestock, including bovine species. This study aimed to investigate TBPs in cattle and ticks across four sampling points, utilizing real-time microfluidic PCR. The results revealed that Rhipicephalus microplus ticks were found infesting all animals. Among [...] Read more.
Tick-borne pathogens (TBPs) pose a significant threat to livestock, including bovine species. This study aimed to investigate TBPs in cattle and ticks across four sampling points, utilizing real-time microfluidic PCR. The results revealed that Rhipicephalus microplus ticks were found infesting all animals. Among the detected TBPs in cattle, Anaplasma marginale was the most frequently identified, often as a single infection, although mixed infections involving Rickettsia felis, uncharacterized Rickettsia sp., and Anaplasma sp. were also observed. In ticks, A. marginale was predominant, along with R. felis, Rickettsia sp., and Ehrlichia sp. It is noteworthy that although A. marginale consistently infected all cattle during various sampling times, this pathogen was not detected in all ticks. This suggests a complex dynamic of pathogen acquisition by ticks. A phylogenetic analysis focused on the identification of Anaplasma species using amplified 16S rDNA gene fragments revealed the presence of A. marginale and Anaplasma platys strains in bovines. These findings underscore the presence of multiple TBPs in both cattle and ticks, with A. marginale being the most prevalent. Understanding the dynamics and phylogenetics of TBPs is crucial for developing effective control strategies to mitigate tick-borne diseases in livestock. Full article
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22 pages, 3745 KiB  
Article
Co-Immunization Efficacy of Recombinant Antigens against Rhipicephalus microplus and Hyalomma anatolicumTick Infestations
by Balasamudram Chandrasekhar Parthasarathi, Binod Kumar, S. K. Bhure, Anil Kumar Sharma, Manisha, Gaurav Nagar, Sachin Kumar, Abhijit Nandi, Haranahally Vasanthachar Manjunathachar, Gajanan M. Chigure, Mukesh Shakya, Muthu Sankar, José de la Fuente and Srikant Ghosh
Pathogens 2023, 12(3), 433; https://doi.org/10.3390/pathogens12030433 - 09 Mar 2023
Cited by 3 | Viewed by 1995
Abstract
The immunoprophylactic management of ticks is the most effective option to control tick infestations and counter spread the acaricide resistance problem worldwide. Several researchers reported an inconsistent efficacy of the single antigen-based immunization of hosts against different tick species. In the present study, [...] Read more.
The immunoprophylactic management of ticks is the most effective option to control tick infestations and counter spread the acaricide resistance problem worldwide. Several researchers reported an inconsistent efficacy of the single antigen-based immunization of hosts against different tick species. In the present study, to develop a multi-target immunization protocol, proteins from Rhipicephalus microplus BM86 and Hyalomma anatolicum subolesin (SUB) and tropomyosin (TPM) were targeted to evaluate the cross-protective potential. The sequence identities of the BM86, SUB, and TPM coding genes amongst Indian tick isolates of targeted species were 95.6–99.8%, 98.7–99.6%, and 98.9–99.9%, respectively, while at the predicted amino acid level, the identities were 93.2 to 99.5, 97.6 to 99.4, and 98.2 to 99.3%. The targeted genes were expressed in the eukaryotic expression system, pKLAC2-Kluyveromyces lactis, and 100 µg each of purified recombinant protein (Bm86-89 kDa, SUB-21 kDa, and TPM-36 kDa) mixed with adjuvant was injected individually through the intramuscular route at different sites of the body on days 0, 30, and 60 to immunize cross-bred cattle. Post-immunization, a statistically significant (p < 0.001) antibody response (IgG, IgG1, and IgG2) in comparison to the control, starting from 15 to 140 days, against each antigen was recorded. Following multi-antigen immunization, the animals were challenged twice with the larvae of R. microplus and H. anatolicum and theadults of H. anatolicum, and a significant vaccine efficacy of 87.2% and 86.2% against H. anatolicum larvae and adults, respectively, and 86.7% against R. microplus was obtained. The current study provides significant support to develop a multi-antigen vaccine against cattle tick species. Full article
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2022

Jump to: 2023, 2021, 2020

15 pages, 2781 KiB  
Article
Dynamic Analysis of microRNAs from Different Life Stages of Rhipicephalus microplus (Acari: Ixodidae) by High-Throughput Sequencing
by Jin Luo, Shuaiyang Zhao, Qiaoyun Ren, Qilin Wang, Zeyu Chen, Jingjing Cui, Yujiao Jing, Peiwen Liu, Ruofeng Yan, Xiaokai Song, Guangyuan Liu and Xiangrui Li
Pathogens 2022, 11(10), 1148; https://doi.org/10.3390/pathogens11101148 - 04 Oct 2022
Cited by 1 | Viewed by 1862
Abstract
MicroRNAs (miRNAs), which are small, noncoding RNA molecules, play an important regulatory role in gene expression at the posttranscriptional level. Relatively limited knowledge exists on miRNAs in Rhipicephalus microplus ticks in China; however, understanding the physiology of miRNA functions and expression at different [...] Read more.
MicroRNAs (miRNAs), which are small, noncoding RNA molecules, play an important regulatory role in gene expression at the posttranscriptional level. Relatively limited knowledge exists on miRNAs in Rhipicephalus microplus ticks in China; however, understanding the physiology of miRNA functions and expression at different developmental stages is important. In this study, three small RNA libraries were constructed for R. microplus eggs, larvae, and female adults; miRNAs were detected during these developmental stages by high-throughput sequencing, with 18,162,337, 8,090,736, and 11,807,326 clean reads, respectively. A total of 5132 known miRNAs and 31 novel miRNAs were identified. A total of 1736 differentially expressed miRNAs were significantly different at a p-value of <0.01; in female adults, 467 microRNAs were upregulated and 376 miRNAs downregulated compared to larval tick controls. Using larvae as controls, 218 upregulated and 203 downregulated miRNAs were detected in eggs; in eggs, 108 miRNAs were upregulated and 364 downregulated compared to female adults controls. To verify the reliability of the sequencing data, RT–qPCR was applied to compare expression levels of novel miRNAs. Some differentially expressed miRNAs are involved in developmental physiology, signal transduction, and cell-extracellular communications based on GO annotation and KEGG pathway analyses. Here, we provide a dynamic analysis of miRNAs in R. microplus and their potential targets, which has significance for understanding the biology of ticks and lays the foundation for improved understanding of miRNA functioning in the regulation of R. microplus development. These results can assist future miRNA studies in other tick species that have great significance for human and animal health. Full article
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13 pages, 518 KiB  
Article
Borrelia burgdorferi Migration Assays for Evaluation of Chemoattractants in Tick Saliva
by Mary B. Jacobs, Britton J. Grasperge, Lara A. Doyle-Meyers and Monica E. Embers
Pathogens 2022, 11(5), 530; https://doi.org/10.3390/pathogens11050530 - 01 May 2022
Cited by 2 | Viewed by 2080
Abstract
Uptake of the Lyme disease spirochete by its tick vector requires not only chemical signals present in the tick’s saliva but a responsive phenotype by the Borrelia burgdorferi living in the mammalian host. This is the principle behind xenodiagnosis, wherein pathogen is detected [...] Read more.
Uptake of the Lyme disease spirochete by its tick vector requires not only chemical signals present in the tick’s saliva but a responsive phenotype by the Borrelia burgdorferi living in the mammalian host. This is the principle behind xenodiagnosis, wherein pathogen is detected by vector acquisition. To study migration of B. burgdorferi toward Ixodes scapularis tick saliva, with the goal of identifying chemoattractant molecules, we tested multiple assays and compared migration of host-adapted spirochetes to those cultured in vitro. We tested mammalian host-adapted spirochetes, along with those grown in culture at 34 °C, for their relative attraction to tick saliva or the nutrient N-acetyl-D-glucosamine (D-GlcNAc) and its dimer chitobiose using two different experimental designs. The host-adapted B. burgdorferi showed greater preference for tick saliva over the nutrients, whereas the cultured incubator-grown B. burgdorferi displayed no significant attraction to saliva versus a significant response to the nutrients. Our results not only describe a validated migration assay for studies of the Lyme disease agent, but provide a further understanding of how growth conditions and phenotype of B. burgdorferi are related to vector acquisition. Full article
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2021

Jump to: 2023, 2022, 2020

19 pages, 2334 KiB  
Opinion
Pitfalls in Tick and Tick-Borne Pathogens Research, Some Recommendations and a Call for Data Sharing
by Agustín Estrada-Peña, Aitor Cevidanes, Hein Sprong and Javier Millán
Pathogens 2021, 10(6), 712; https://doi.org/10.3390/pathogens10060712 - 07 Jun 2021
Cited by 15 | Viewed by 4984
Abstract
An understanding of the relationships of ticks and tick-borne pathogens can only be achieved by integrating data from multiple studies. The publication of raw material is a necessary step for wide-area meta-analyses and study design, data collection and reporting require harmonization. This is [...] Read more.
An understanding of the relationships of ticks and tick-borne pathogens can only be achieved by integrating data from multiple studies. The publication of raw material is a necessary step for wide-area meta-analyses and study design, data collection and reporting require harmonization. This is an opinion paper, not a consensus position, and is open to debate. This work reflects our view about how data should be communicated in mainstream journals. We indicate rules that should be observed in recording weather data, to avoid serendipitous correlations between the density of ticks and climate variables and recommend the inclusion of raw data in reports. We stress the need for standardized methods to collect ticks that cannot be obtained by standard flagging. The reporting of infection rates of pathogens in ticks should avoid conclusions based on pure molecular findings in feeding ticks. Studies demonstrating the vectorial capacity of ticks should not be supported only by molecular surveys of feeding ticks. Vacuous conclusions about vectorial or reservoir status based solely on the finding of genomic material of a pathogen should be discouraged. We stress that phylogenetic studies based on random selection of sequences from GenBank are unsuitable. We firmly support the development of a dedicated server of curated sequences of ticks and pathogens as a standard for future studies. Full article
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16 pages, 3213 KiB  
Article
Tick Importin-α Is Implicated in the Interactome and Regulome of the Cofactor Subolesin
by Sara Artigas-Jerónimo, Margarita Villar, Alejandro Cabezas-Cruz, Grégory Caignard, Damien Vitour, Jennifer Richardson, Sandrine Lacour, Houssam Attoui, Lesley Bell-Sakyi, Eleonore Allain, Ard M. Nijhof, Nina Militzer, Sophia Pinecki Socias and José de la Fuente
Pathogens 2021, 10(4), 457; https://doi.org/10.3390/pathogens10040457 - 11 Apr 2021
Cited by 4 | Viewed by 2998
Abstract
Ticks and tick-borne diseases (TBDs) represent a burden for human and animal health worldwide. Currently, vaccines constitute the safest and most effective approach to control ticks and TBDs. Subolesin (SUB) has been identified as a vaccine antigen for the control of tick infestations [...] Read more.
Ticks and tick-borne diseases (TBDs) represent a burden for human and animal health worldwide. Currently, vaccines constitute the safest and most effective approach to control ticks and TBDs. Subolesin (SUB) has been identified as a vaccine antigen for the control of tick infestations and pathogen infection and transmission. The characterization of the molecular function of SUB and the identification of tick proteins interacting with SUB may provide the basis for the discovery of novel antigens and for the rational design of novel anti-tick vaccines. In the present study, we used the yeast two-hybrid system (Y2H) as an unbiased approach to identify tick SUB-interacting proteins in an Ixodes ricinus cDNA library, and studied the possible role of SUB as a chromatin remodeler through direct interaction with histones. The Y2H screening identified Importin-α as a potential SUB-interacting protein, which was confirmed in vitro in a protein pull-down assay. The sub gene expression levels in tick midgut and fat body were significantly higher in unfed than fed female ticks, however, the importin-α expression levels did not vary between unfed and fed ticks but tended to be higher in the ovary when compared to those in other organs. The effect of importin-α RNAi was characterized in I. ricinus under artificial feeding conditions. Both sub and importin-α gene knockdown was observed in all tick tissues and, while tick weight was significantly lower in sub RNAi-treated ticks than in controls, importin-α RNAi did not affect tick feeding or oviposition, suggesting that SUB is able to exert its function in the absence of Importin-α. Furthermore, SUB was shown to physically interact with histone 4, which was corroborated by protein pull-down and western blot analysis. These results confirm that by interacting with numerous tick proteins, SUB is a key cofactor of the tick interactome and regulome. Further studies are needed to elucidate the nature of the SUB-Importin-α interaction and the biological processes and functional implications that this interaction may have. Full article
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19 pages, 1253 KiB  
Article
Development of a Multiplex PCR and Magnetic DNA Capture Assay for Detecting Six Species Pathogens of the Genera Anaplasma and Ehrlichia in Canine, Bovine, Caprine and Ovine Blood Samples from Grenada, West Indies
by Bhumika Sharma, Roman R. Ganta, Diana Stone, Andy Alhassan, Marta Lanza-Perea, Vanessa Matthew Belmar, Inga Karasek, Elizabeth Cooksey, Catherine M. Butler, Kathryn Gibson and Melinda J. Wilkerson
Pathogens 2021, 10(2), 192; https://doi.org/10.3390/pathogens10020192 - 10 Feb 2021
Cited by 7 | Viewed by 3156
Abstract
Infections with tick-borne pathogens belonging to Anaplasma/Ehrlichia in various vertebrate hosts are a persistent problem resulting in nonspecific clinical signs during early infection. Diagnosis of single and multi-infections with these pathogens, causing diseases in companion/agricultural animals and people, remains a challenge. Traditional methods [...] Read more.
Infections with tick-borne pathogens belonging to Anaplasma/Ehrlichia in various vertebrate hosts are a persistent problem resulting in nonspecific clinical signs during early infection. Diagnosis of single and multi-infections with these pathogens, causing diseases in companion/agricultural animals and people, remains a challenge. Traditional methods of diagnosis, such as microscopy and serology, have low sensitivity and specificity. Polymerase chain reaction (PCR) assays are widely used to detect early-phase infections, since these have high sensitivity and specificity. We report the development and validation of an assay involving PCR followed by magnetic capture method using species-specific oligonucleotides to detect six Anaplasma/Ehrlichia species pathogens in canine, bovine, caprine, and ovine blood samples. Overall, the assay application to 455 samples detected 30.1% (137/455) positives for one or more out of six screened pathogens. Single-pathogen infections were observed in 94.9% (130/137) of the positive samples, while co-infections were detected in 5.1% (7/137). Anaplasma marginale infection in cattle had the highest detection rate (34.4%), followed by canines positive for Anaplasma platys (16.4%) and Ehrlichia canis (13.9%). The assay aided in documenting the first molecular evidence for A. marginale in cattle and small ruminants and Ehrlichia chaffeensis and Ehrlichia ewingii in dogs in the Caribbean island of Grenada. Full article
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18 pages, 760 KiB  
Article
Characterization of the Rhipicephalus (Boophilus) microplus Sialotranscriptome Profile in Response to Theileria equi Infection
by Patrícia Paulino, Gabriela Vitari, Antonio Rezende, Joana Couto, Sandra Antunes, Ana Domingos, Maristela Peckle, Carlos Massard, Flávio Araújo and Huarrisson Santos
Pathogens 2021, 10(2), 167; https://doi.org/10.3390/pathogens10020167 - 04 Feb 2021
Cited by 5 | Viewed by 2370
Abstract
This study intends to characterize the sialotranscriptome profile of Rhipicephalus (Boophilus) microplus in response to Theileria equi and identify genes of interest with differential genomic expression, indicating relevant targets in the tick–protozoan interactions. The experimental design consisted of RNA sequencing from uninfected and [...] Read more.
This study intends to characterize the sialotranscriptome profile of Rhipicephalus (Boophilus) microplus in response to Theileria equi and identify genes of interest with differential genomic expression, indicating relevant targets in the tick–protozoan interactions. The experimental design consisted of RNA sequencing from uninfected and T. equi-infected R. microplus salivary glands (SGs) to obtain transcriptomic profiles for characterization and comparison. A total of 288,952 transcripts were obtained from both tick profiles, 3456 transcripts (p < 0.05) differentially expressed in response to T. equi infection. The uninfected SGs’ registered 231,179 transcripts, of which 155,359 were annotated. The most transcribed sequences were female-specific histamine binding protein and lipocalins. Regarding the T. equi-infected SGs, from the 238,964 assembled transcripts, 163,564 were annotated. The most transcribed sequences were histone demethylase JARID1 and Y-box-binding protein. Five transcripts (cystatin, arginase, nuclear factor κB kinase inhibitor subunit β (IκB), IκB delta, lysosomal-trafficking regulator, and reeler protein) presented the gene ontology (GO) category “response to protozoan” and were exclusively displayed in the T. equi-infected profile. The transcriptome of T. equi was also analyzed, registering 4728 hits. The study’s genetic and molecular information would be of great value for future studies and biotechnological applications envisaging disease control. Full article
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31 pages, 989 KiB  
Review
Challenges in Tick-Borne Pathogen Detection: The Case for Babesia spp. Identification in the Tick Vector
by Grecia Martínez-García, R. Montserrat Santamaría-Espinosa, José J. Lira-Amaya and Julio V. Figueroa
Pathogens 2021, 10(2), 92; https://doi.org/10.3390/pathogens10020092 - 20 Jan 2021
Cited by 20 | Viewed by 4427
Abstract
The causative agents of Babesiosis are intraerythrocytic protozoa of the genus Babesia. Babesia parasites are present around the world, affecting several mammals including humans, pets and livestock, hence its medical and veterinary relevance. Babesia spp. detection in its invertebrate host is a [...] Read more.
The causative agents of Babesiosis are intraerythrocytic protozoa of the genus Babesia. Babesia parasites are present around the world, affecting several mammals including humans, pets and livestock, hence its medical and veterinary relevance. Babesia spp. detection in its invertebrate host is a main point in understanding the biology of the parasite to acquire more knowledge on the host–Babesia–vector interactions, as increasing knowledge of the Babesia lifecycle and babesiosis epidemiology can help prevent babesiosis outbreaks in susceptible mammals. The aim of the present review is to highlight the newest findings in this field, based on a bibliographic compilation of research studies recently carried out for the detection of the main Babesia species found in tick vectors affecting mammalian hosts, including the different tick stages such as adult ticks, larvae, nymphs and eggs, as well as the detection method implemented: microscopic tools for parasite identification and molecular tools for parasite DNA detection by conventional PCR, nested-PCR, PCR-RFLP, PCR-RLB hybridization, real time-PCR, LAMP and RAP assays. Although molecular identification of Babesia parasites has been achieved in several tick species and tissue samples, it is still necessary to carry out transmission experiments through biological models to confirm the vectorial capacity of various tick species. Full article
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2020

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9 pages, 783 KiB  
Article
Closing the Gaps to Understand the Tick Transmission of Anaplasma marginale among Giant Anteaters (Myrmecophaga tridactyla) in Argentina
by Eliana Carolina Guillemi, Mélody Imbert, Sofia de la Fournière, María Marcela Orozco, Jorge Peña Martinez, Ana Carolina Rosas, Valeria Noely Montenegro and Marisa Diana Farber
Pathogens 2020, 9(12), 1033; https://doi.org/10.3390/pathogens9121033 - 09 Dec 2020
Cited by 2 | Viewed by 2016
Abstract
Anaplasma marginale, a well-known cattle pathogen of tropical and subtropical world regions, has been previously molecularly characterized in a giant anteater (Myrmecophaga tridactyla) from Corrientes, Argentina. Ticks or other hematophagous arthropod involved in the wild transmission cycle remained unknown. The [...] Read more.
Anaplasma marginale, a well-known cattle pathogen of tropical and subtropical world regions, has been previously molecularly characterized in a giant anteater (Myrmecophaga tridactyla) from Corrientes, Argentina. Ticks or other hematophagous arthropod involved in the wild transmission cycle remained unknown. The aim of the present study was to analyze the simultaneous occurrence of A. marginale in blood samples and ticks from giant anteaters from Corrientes in order to investigate if ticks could be relevant in the transmission among these mammals. Blood samples from 50 giant anteaters collected in different years and 26 ticks Amblyomma dubitatum and A. sculptum were studied through the molecular amplification of two unequivocal species-specific genes from A. marginale: msp5 and msp1β. Twenty five giant anteaters and tick organs (salivary glands, gut and oviduct) from 11 ticks tested positive to the A. marginale DNA amplification. The further molecular characterization through MSP1a tandem repeats analysis revealed the presence of genotypes circulating among giant anteaters that had been previously identified in cattle blood samples from the same geographical region. These results confirm the presence of A. marginale in giant anteaters in Corrientes and suggests that A. dubitatum and A. sculptum ticks could be involved in the transmission among giant anteaters. Future studies will determine the role of these tick species in the wild transmission cycle in the study area and the eventual connection with the domestic cycle. Full article
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11 pages, 758 KiB  
Article
Anaplasma phagocytophilum and Babesia Species of Sympatric Roe Deer (Capreolus capreolus), Fallow Deer (Dama dama), Sika Deer (Cervus nippon) and Red Deer (Cervus elaphus) in Germany
by Cornelia Silaghi, Julia Fröhlich, Hubert Reindl, Dietmar Hamel and Steffen Rehbein
Pathogens 2020, 9(11), 968; https://doi.org/10.3390/pathogens9110968 - 20 Nov 2020
Cited by 13 | Viewed by 2344
Abstract
(1) Background: Wild cervids play an important role in transmission cycles of tick-borne pathogens; however, investigations of tick-borne pathogens in sika deer in Germany are lacking. (2) Methods: Spleen tissue of 74 sympatric wild cervids (30 roe deer, 7 fallow deer, 22 sika [...] Read more.
(1) Background: Wild cervids play an important role in transmission cycles of tick-borne pathogens; however, investigations of tick-borne pathogens in sika deer in Germany are lacking. (2) Methods: Spleen tissue of 74 sympatric wild cervids (30 roe deer, 7 fallow deer, 22 sika deer, 15 red deer) and of 27 red deer from a farm from southeastern Germany were analyzed by molecular methods for the presence of Anaplasma phagocytophilum and Babesia species. (3) Results: Anaplasma phagocytophilum and Babesia DNA was demonstrated in 90.5% and 47.3% of the 74 combined wild cervids and 14.8% and 18.5% of the farmed deer, respectively. Twelve 16S rRNA variants of A. phagocytophilum were delineated. While the infection rate for A. phagocytophilum among the four cervid species was similar (71.4% to 100%), it varied significantly for Babesia between roe deer (73.3%), fallow deer (14.3%), sika deer (27.3%) and red deer (40.0%). Deer ≤2 years of age tested significantly more often positive than the older deer for both A. phagocytophilum and Babesia species. (4) Conclusions: This study confirms the widespread occurrence of A. phagocytophilum and Babesia species in wild cervids and farmed red deer in Germany and documents the co-occurrence of the two tick-borne pathogens in free-ranging sika deer. Full article
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30 pages, 1494 KiB  
Review
Systematic Review of Ticks and Tick-Borne Pathogens of Small Ruminants in Pakistan
by Abdul Ghafar, Tariq Abbas, Abdul Rehman, Zia-ud-Din Sandhu, Alejandro Cabezas-Cruz and Abdul Jabbar
Pathogens 2020, 9(11), 937; https://doi.org/10.3390/pathogens9110937 - 11 Nov 2020
Cited by 19 | Viewed by 7531
Abstract
Ticks and tick-borne diseases (TTBDis) are a major constraint to the health and production of small ruminants in Pakistan. Despite being the subject of intermittent studies over the past few decades, comprehensive information on the epidemiology and control of TTBDis is lacking. Herein, [...] Read more.
Ticks and tick-borne diseases (TTBDis) are a major constraint to the health and production of small ruminants in Pakistan. Despite being the subject of intermittent studies over the past few decades, comprehensive information on the epidemiology and control of TTBDis is lacking. Herein, we have systematically reviewed the current knowledge on TTBDis of small ruminants in Pakistan. Critical appraisal of the selected 71 articles published between 1947 to 2020 revealed that morphological examination had been the most widely used method for the identification of TTBDis in Pakistan. Tick fauna comprise at least 40 species, mainly belonging to Haemaphysalis, Hyalomma and Rhipicephalus. The prevalence of ticks is the highest in summer (June–September) and it is also higher in goats than sheep. Anaplasma, Babesia and Theileria spp. are the major tick-borne pathogens (TBPs), and their prevalence is usually higher in sheep than goats. Spatio-temporal distribution, genetic diversity and control of ticks and TBPs of small ruminants as well as the competence of tick vectors for various TBPs remain to be explored. Therefore, coordinated and focused investigations are required to fill knowledge gaps in these areas to maximise the health, production and welfare of small ruminants and minimise economic losses associated with TTBDis in Pakistan. Full article
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18 pages, 3086 KiB  
Article
Molecular Diagnosis, Prevalence and Importance of Zoonotic Vector-Borne Pathogens in Cuban Shelter Dogs—A Preliminary Study
by Adrian Alberto Díaz-Sánchez, Belkis Corona-González, Marina L. Meli, Lisset Roblejo-Arias, Osvaldo Fonseca-Rodríguez, Anisleidy Pérez Castillo, Ernesto Vega Cañizares, Evelyn Lobo Rivero and Regina Hofmann-Lehmann
Pathogens 2020, 9(11), 901; https://doi.org/10.3390/pathogens9110901 - 28 Oct 2020
Cited by 8 | Viewed by 2634
Abstract
The present study aimed to determine the prevalence of zoonotic vector-borne pathogens, including Anaplasma platys, Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, Ehrlichia canis and Rickettsia spp. in shelter dogs from Cuba. Blood samples were collected from 100 shelter dogs and examined [...] Read more.
The present study aimed to determine the prevalence of zoonotic vector-borne pathogens, including Anaplasma platys, Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, Ehrlichia canis and Rickettsia spp. in shelter dogs from Cuba. Blood samples were collected from 100 shelter dogs and examined by molecular methods. Overall, 85 (85%; 95% CI: 77.88–92.12) dogs tested positive for at least one vector-borne pathogen using species-specific qPCR assays. Among the positive samples, E. canis was the most prevalent 62% (95% CI: 52.32–71.68), followed by A. platys 40% (95% CI: 30.23–49.77) and Rickettsia felis 27% (95% CI: 18.15–35.85), whereas 36% (95% CI: 26.43–45.57) showed co-infections. All samples were negative for A. phagocytophilum and B. burgdorferi s.l. The presence of 248 Rhipicephalus sanguineus ticks collected from the dogs was not statistically associated with the occurrence of infections. Thrombocytopenia was the most frequent haematological alteration found in PCR-positive dogs; it was statistically associated with the presence of E. canis, as well as co-infections (p < 0.05). The phylogenetic analyses of A. platys and E. canis based on 16S rRNA, groEL and gltA genes showed a low genetic diversity between Cuban strains. The present study demonstrates the high prevalence of vector-borne pathogens with zoonotic potential in shelter dogs from Cuba. Full article
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16 pages, 25265 KiB  
Article
Multiple Antigenic Peptide-Based Vaccines Targeting Ixodes ricinus Neuropeptides Induce a Specific Antibody Response but Do Not Impact Tick Infestation
by Consuelo Almazán, Ladislav Šimo, Lisa Fourniol, Sabine Rakotobe, Jérémie Borneres, Martine Cote, Sandy Peltier, Jennifer Mayé, Nicolas Versillé, Jennifer Richardson and Sarah I. Bonnet
Pathogens 2020, 9(11), 900; https://doi.org/10.3390/pathogens9110900 - 28 Oct 2020
Cited by 9 | Viewed by 2567
Abstract
Synthetic peptide vaccines were designed to target the neuropeptides innervating Ixodes ricinus salivary glands and hindgut and they were tested for their capacity to afford protective immunity against nymphs or larvae and Anaplasma phagocytophilum-infected nymph infestation, in mice and sheep, respectively. In [...] Read more.
Synthetic peptide vaccines were designed to target the neuropeptides innervating Ixodes ricinus salivary glands and hindgut and they were tested for their capacity to afford protective immunity against nymphs or larvae and Anaplasma phagocytophilum-infected nymph infestation, in mice and sheep, respectively. In both models, the assembly of SIFamide (SIFa) or myoinhibitory peptide (MIP) neuropeptides into multiple antigenic peptide constructs (MAPs) elicited a robust IgG antibody response following immunization. Nevertheless, no observable detrimental impact on nymphs was evidenced in mice, and, unfortunately, the number of engorged nymphs on sheep was insufficient for firm conclusions to be drawn, including for bacterial transmission. Regarding larvae, while vaccination of the sheep did not globally diminish tick feeding success or development, analyses of animals at the individual level revealed a negative correlation between anti-SIFa and MIP antibody levels and larva-to-nymph molting success for both antigens. Our results provide a proof of principle and precedent for the use of MAPs for the induction of immunity against tick peptide molecules. Although the present study did not provide the expected level of protection, it inaugurates a new strategy for protection against ticks based on the immunological targeting of key components of their nervous system. Full article
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13 pages, 967 KiB  
Article
Bovines Harbor a Diverse Array of Vector-Borne Pathogens in Northeast Algeria
by Ghania Boularias, Naouelle Azzag, Christelle Gandoin, Corinne Bouillin, Bruno Chomel, Nadia Haddad and Henri-Jean Boulouis
Pathogens 2020, 9(11), 883; https://doi.org/10.3390/pathogens9110883 - 25 Oct 2020
Cited by 5 | Viewed by 2394
Abstract
Arthropod-borne hemoparasites represent a serious health problem in livestock, causing significant production losses. Currently, the evidence of Anaplasma spp., Theileria spp., Babesia spp., and hemotropic Mycoplasma spp. in Algeria remains limited to a few scattered geographical regions. In this work, our objectives were [...] Read more.
Arthropod-borne hemoparasites represent a serious health problem in livestock, causing significant production losses. Currently, the evidence of Anaplasma spp., Theileria spp., Babesia spp., and hemotropic Mycoplasma spp. in Algeria remains limited to a few scattered geographical regions. In this work, our objectives were to study the prevalence of these vector-borne pathogens and to search other agents not yet described in Algeria as well as the identification of statistical associations with various risk factors in cattle in the northeast of Algeria. Among the 205 cattle blood samples tested by PCR analysis, 42.4% positive results were obtained for at least one pathogen. The overall rates of Anaplasma spp., Theileria/Babesia spp., and Mycoplasma spp. in the cattle sampled were respectively 30.7%, 18.5%, and 2.9%; co-infections with multiple species was also detected. Anaplasma spp. and Theileria/Babesia spp. were detected at a higher rate in cattle under 3 years old, according to univariate analysis. Anaplasma spp. DNA was detected more frequently in our sample in cattle living in semi extensive farming. Our study provides additional data about Anaplasma spp., Theileria/Babesia spp. and reveals for the first time that Mycoplasma wenyonii and ‘Candidatus Mycoplasma hemobos are present in cattle in Northeast Algeria. Full article
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15 pages, 1288 KiB  
Article
Transstadial Transmission and Replication Kinetics of West Nile Virus Lineage 1 in Laboratory Reared Ixodes ricinus Ticks
by Cristian Răileanu, Oliver Tauchmann, Ana Vasić, Ulrike Neumann, Birke Andrea Tews and Cornelia Silaghi
Pathogens 2020, 9(10), 780; https://doi.org/10.3390/pathogens9100780 - 24 Sep 2020
Cited by 2 | Viewed by 3337
Abstract
West Nile virus (WNV) is a mosquito-borne agent that has also been isolated from several tick species. Vector competence of Ixodes ricinus, one of the most common tick species in Europe, has been poorly investigated for WNV to date. As such, to [...] Read more.
West Nile virus (WNV) is a mosquito-borne agent that has also been isolated from several tick species. Vector competence of Ixodes ricinus, one of the most common tick species in Europe, has been poorly investigated for WNV to date. As such, to evaluate the vector competence, laboratory reared Ixodes ricinus nymphs were in vitro fed with WNV lineage 1 infectious blood, allowed to molt, and the resulting females artificially fed to study the virus transmission. Furthermore, we studied the kinetics of WNV replication in ticks after infecting nymphs using an automatic injector. Active replication of WNV was detected in injected nymphs from day 7 post-infection until 28 dpi. In the nymphs infected by artificial feeding, the transstadial transmission of WNV was confirmed molecularly in 46.7% of males, while virus transmission during in vitro feeding of I. ricinus females originating from infected nymphs was not registered. The long persistence of WNV in I. ricinus ticks did not correlate with the transmission of the virus and it is unlikely that I. ricinus represents a competent vector. However, there is a potential reservoir role that this tick species can play, with hosts potentially acquiring the viral agent after ingesting the infected ticks. Full article
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24 pages, 2145 KiB  
Review
Ticks and Tick-Borne Diseases in Cuba, Half a Century of Scientific Research
by Dasiel Obregón Alvarez, Belkis Corona-González, Alina Rodríguez-Mallón, Islay Rodríguez Gonzalez, Pastor Alfonso, Angel A. Noda Ramos, Adrian A. Díaz-Sánchez, Maylin González Navarrete, Rafmary Rodríguez Fernández, Luis Méndez Mellor, Helen N. Catanese, Manuel Peláez, Yousmel Alemán Gainza, Roxana Marrero-Perera, Lisset Roblejo-Arias, Evelyn Lobo-Rivero, Claudia B. Silva, Adivaldo H. Fonseca, Eugenio Roque López and Alejandro Cabezas-Cruz
Pathogens 2020, 9(8), 616; https://doi.org/10.3390/pathogens9080616 - 28 Jul 2020
Cited by 16 | Viewed by 5853
Abstract
Ticks and the vast array of pathogens they transmit, including bacteria, viruses, protozoa, and helminths, constitute a growing burden for human and animal health worldwide. In Cuba, the major tropical island in the Caribbean, ticks are an important cause of vector-borne diseases affecting [...] Read more.
Ticks and the vast array of pathogens they transmit, including bacteria, viruses, protozoa, and helminths, constitute a growing burden for human and animal health worldwide. In Cuba, the major tropical island in the Caribbean, ticks are an important cause of vector-borne diseases affecting livestock production, pet animal health and, to a lesser extent, human health. The higher number of tick species in the country belong to the Argasidae family and, probably less known, is the presence of an autochthonous tick species in the island, Ixodes capromydis. Herein, we provide a comprehensive review of the ticks and tick-borne pathogens (TBPs) affecting animal and human health in Cuba. The review covers research results including ecophysiology of ticks, the epidemiology of TBPs, and the diagnostic tools used currently in the country for the surveillance of TBPs. We also introduce the programs implemented in the country for tick control and the biotechnology research applied to the development of anti-tick vaccines. Full article
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10 pages, 818 KiB  
Article
Dermacentor reticulatus and Babesia canis in Bavaria (Germany)—A Georeferenced Field Study with Digital Habitat Characterization
by Cornelia Silaghi, Lisa Weis and Kurt Pfister
Pathogens 2020, 9(7), 541; https://doi.org/10.3390/pathogens9070541 - 07 Jul 2020
Cited by 17 | Viewed by 2796
Abstract
The hard tick Dermacentor reticulatus transmits Babesia canis, the causative agent of canine babesiosis. Both the occurrence and local distribution of D. reticulatus as well as infection rates of questing ticks with B. canis are thus far poorly known in Bavaria, Germany. [...] Read more.
The hard tick Dermacentor reticulatus transmits Babesia canis, the causative agent of canine babesiosis. Both the occurrence and local distribution of D. reticulatus as well as infection rates of questing ticks with B. canis are thus far poorly known in Bavaria, Germany. The objectives of this study were to conduct (1) a georeferenced field study on the occurrence of D. reticulatus with digital habitat characterization and (2) a PCR analysis of D. reticulatus collected in Bavaria for infection with B. canis. Dermacentor reticulatus were collected by flagging at 60 sites specifically selected according to habitat conditions and screened individually for Babesia DNA. A digital habitat characterization for D. reticulatus was performed according to results of the field analysis including the parameters land use, proximity to water, “potential natural vegetation”, red deer corridors and climate data. Altogether, 339 D. reticulatus ticks (214 females and 125 males) were collected between 2010 and 2013 at 12 out of 60 sampling sites. All 12 sites were characterized by high humidity with marshy areas. Babesia canis DNA was detected in 1 out of 301 (0.3%) questing D. reticulatus in Bavaria. The digital habitat characterization revealed 15 forest areas in Bavaria with similar ecological characteristics as the sites positive for D. reticulatus. Full article
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26 pages, 3708 KiB  
Article
Functional and Mass Spectrometric Evaluation of an Anti-Tick Antigen Based on the P0 Peptide Conjugated to Bm86 Protein
by Alina Rodríguez Mallón, Luis Javier González, Pedro Enrique Encinosa Guzmán, Gervasio Henrique Bechara, Gustavo Seron Sanches, Satomy Pousa, Gleysin Cabrera, Ania Cabrales, Hilda Garay, Raúl Mejías, José Raúl López Álvarez, Yamil Bello Soto, Fabiola Almeida, Osmany Guirola, Rafmary Rodríguez Fernández, Alier Fuentes Castillo, Luis Méndez, Samanta Jiménez, Alexei Licea-Navarro, Madelón Portela, Rosario Durán and Mario Pablo Estradaadd Show full author list remove Hide full author list
Pathogens 2020, 9(6), 513; https://doi.org/10.3390/pathogens9060513 - 25 Jun 2020
Cited by 20 | Viewed by 3377
Abstract
A synthetic 20 amino acid peptide of the ribosomal protein P0 from ticks, when conjugated to keyhole limpet hemocyanin from Megathura crenulata and used as an immunogen against Rhipicephalus microplus and Rhipicephalus sanguineus s.l. species, has shown efficacies of around 90%. There is [...] Read more.
A synthetic 20 amino acid peptide of the ribosomal protein P0 from ticks, when conjugated to keyhole limpet hemocyanin from Megathura crenulata and used as an immunogen against Rhipicephalus microplus and Rhipicephalus sanguineus s.l. species, has shown efficacies of around 90%. There is also experimental evidence of a high efficacy of this conjugate against Amblyomma mixtum and Ixodes ricinus species, which suggest that this antigen could be a good broad-spectrum anti-tick vaccine candidate. In this study, the P0 peptide (pP0) was chemically conjugated to Bm86 as a carrier protein. SDS-PAGE analysis of this conjugate demonstrated that it is highly heterogeneous in size, carrying from 1 to 18 molecules of pP0 per molecule of Bm86. Forty-nine out of the 54 lysine residues and the N-terminal end of Bm86 were found partially linked to pP0 by using LC-MS/MS analysis and the combination of four different softwares. Several post-translational modifications of Bm86 protein were also identified by mass spectrometry. High immunogenicity and efficacy were achieved when dogs and cattle were vaccinated with the pP0–Bm86 conjugate and challenged with R. sanguineus s.l. and R. microplus, respectively. These results encourage the development of this antigen with promising possibilities as an anti-tick vaccine. Full article
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11 pages, 3295 KiB  
Article
A Retrospective Assessment of Temperature Trends in Northern Europe Reveals a Deep Impact on the Life Cycle of Ixodes ricinus (Acari: Ixodidae)
by Agustin Estrada-Peña and Natalia Fernández-Ruiz
Pathogens 2020, 9(5), 345; https://doi.org/10.3390/pathogens9050345 - 01 May 2020
Cited by 7 | Viewed by 3650
Abstract
This study modelled the changes in the development processes of the health-threatening tick Ixodes ricinus in Northern Europe as driven by the trends of temperature (1950–2018). We used the ECA&D dataset to calculate the annual accumulated temperature to obtain the development rates of [...] Read more.
This study modelled the changes in the development processes of the health-threatening tick Ixodes ricinus in Northern Europe as driven by the trends of temperature (1950–2018). We used the ECA&D dataset to calculate the annual accumulated temperature to obtain the development rates of the oviposition, incubation, larva–nymph, and nymph–adult molts. Annual values were used to ascertain the trend in development rates of each stage. The ecological classification of Northern Europe (LANMAP2) was used to summarize results. The temperature in 1950–2018 clearly increased in the target territory. The development rates of every tested life cycle process were faster along the time series. Faster oviposition and incubation rates resulted in central Sweden, Baltic countries, and parts of Finland. Faster molting rates were observed in the same territories and in large areas of Western Norway. The trend of temperature in the period 1950–2018 shows a consistent inflection point around 1990, demonstrating that the increased annual accumulated temperature has a deeper impact on the life cycle of I. ricinus since approximately 1990. Faster development rates could be part of the processes driving the reported spread of the tick in the target area and should be considered as a serious threat to human health. Full article
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13 pages, 1257 KiB  
Article
Tripartite Interactions among Ixodiphagus hookeri, Ixodes ricinus and Deer: Differential Interference with Transmission Cycles of Tick-Borne Pathogens
by Aleksandra I. Krawczyk, Julian W. Bakker, Constantianus J. M. Koenraadt, Manoj Fonville, Katsuhisa Takumi, Hein Sprong and Samiye Demir
Pathogens 2020, 9(5), 339; https://doi.org/10.3390/pathogens9050339 - 30 Apr 2020
Cited by 12 | Viewed by 3746
Abstract
For the development of sustainable control of tick-borne diseases, insight is needed in biological factors that affect tick populations. Here, the ecological interactions among Ixodiphagus hookeri, Ixodes ricinus, and two vertebrate species groups were investigated in relation to their effects on [...] Read more.
For the development of sustainable control of tick-borne diseases, insight is needed in biological factors that affect tick populations. Here, the ecological interactions among Ixodiphagus hookeri, Ixodes ricinus, and two vertebrate species groups were investigated in relation to their effects on tick-borne disease risk. In 1129 questing ticks, I. hookeri DNA was detected more often in I. ricinus nymphs (4.4%) than in larvae (0.5%) and not in adults. Therefore, we determined the infestation rate of I. hookeri in nymphs from 19 forest sites, where vertebrate, tick, and tick-borne pathogen communities had been previously quantified. We found higher than expected co-occurrence rates of I. hookeri with deer-associated Anaplasma phagocytophilum, and lower than expected rates with rodent-associated Borrelia afzelii and Neoehrlichia mikurensis. The prevalence of I. hookeri in nymphs varied between 0% and 16% and was positively correlated with the encounter probability of ungulates and the densities of all life stages of I. ricinus. Lastly, we investigated the emergence of I. hookeri from artificially fed, field-collected nymphs. Adult wasps emerged from seven of the 172 fed nymphs. From these observations, we inferred that I. hookeri is parasitizing I. ricinus larvae that are feeding on deer, rather than on rodents or in the vegetation. Since I. hookeri populations depend on deer abundance, the main propagation host of I. ricinus, these wasps have no apparent effect on tick populations. The presence of I. hookeri may directly interfere with the transmission cycle of A. phagocytophilum, but not with that of B. afzelii or N. mikurensis. Full article
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17 pages, 2700 KiB  
Article
Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides
by Agustín Estrada-Peña, Alejandro Cabezas-Cruz and Dasiel Obregón
Pathogens 2020, 9(4), 309; https://doi.org/10.3390/pathogens9040309 - 22 Apr 2020
Cited by 28 | Viewed by 5108
Abstract
Ixodes scapularis ticks harbor microbial communities including pathogenic and non-pathogenic microbes. Pathogen infection increases the expression of several tick gut proteins, which disturb the tick gut microbiota and impact bacterial biofilm formation. Anaplasma phagocytophilum induces ticks to express I. scapularis antifreeze glycoprotein (IAFGP), [...] Read more.
Ixodes scapularis ticks harbor microbial communities including pathogenic and non-pathogenic microbes. Pathogen infection increases the expression of several tick gut proteins, which disturb the tick gut microbiota and impact bacterial biofilm formation. Anaplasma phagocytophilum induces ticks to express I. scapularis antifreeze glycoprotein (IAFGP), a protein with antimicrobial activity, while Borrelia burgdorferi induces the expression of PIXR. Here, we tested the resistance of I. scapularis microbiome to A. phagocytophilum infection, antimicrobial peptide IAFGP, and anti-tick immunity specific to PIXR. We demonstrate that A. phagocytophilum infection and IAFGP affect the taxonomic composition and taxa co-occurrence networks, but had limited impact on the functional traits of tick microbiome. In contrast, anti-tick immunity disturbed the taxonomic composition and the functional profile of tick microbiome, by increasing both the taxonomic and pathways diversity. Mechanistically, we show that anti-tick immunity increases the representation and importance of the polysaccharide biosynthesis pathways involved in biofilm formation, while these pathways are under-represented in the microbiome of ticks infected by A. phagocytophilum or exposed to IAFGP. These analyses revealed that tick microbiota is highly sensitive to anti-tick immunity, while it is less sensitive to pathogen infection and antimicrobial peptides. Results suggest that biofilm formation may be a defensive response of tick microbiome to anti-tick immunity. Full article
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10 pages, 482 KiB  
Article
Efficient Transovarial Transmission of Babesia Spp. in Rhipicephalus microplus Ticks Fed on Water Buffalo (Bubalus bubalis)
by Dasiel Obregón, Belkis Corona-González, Adrian Alberto Díaz-Sánchez, Yasmani Armas, Eugenio Roque, Márcia Cristina de Sena Oliveira and Alejandro Cabezas-Cruz
Pathogens 2020, 9(4), 280; https://doi.org/10.3390/pathogens9040280 - 11 Apr 2020
Cited by 8 | Viewed by 3083
Abstract
Water buffaloes can be infected by tick-borne pathogens (TBPs) in endemic areas where cattle and buffalo coexist. Among TBPs affecting buffaloes is the Apicomplexan hemoparasites Babesia bovis and B. bigemina, transmitted by Rhipicephalus microplus ticks. However, little empirical evidence exists on whether [...] Read more.
Water buffaloes can be infected by tick-borne pathogens (TBPs) in endemic areas where cattle and buffalo coexist. Among TBPs affecting buffaloes is the Apicomplexan hemoparasites Babesia bovis and B. bigemina, transmitted by Rhipicephalus microplus ticks. However, little empirical evidence exists on whether buffalo can support TBPs’ infection and transmission. A cohort study was designed to measure the infestation levels of R. microplus in buffaloes as well as the ability of buffalo-fed ticks to transmit B. bovis and B. bigemina to their offspring. Tick infestation of different life stages was quantified in cattle and buffalo kept in field conditions in western Cuba. Engorged adult female ticks were allowed to lay eggs in controlled conditions of humidity and temperature, and reproductive parameters were measured and analyzed. Hosts and tick larvae were tested for the presence of Babesia spp. using species-specific qPCR assays. Tick infestation was not observed in adult buffaloes. However, buffalo and cattle calves were equally infested, although the larval survival rate was higher in cattle calves than in buffalo calves. All larval pools (31) obtained from the adult female ticks were positive for B. bovis, whereas only 68% (21/31) was positive for B. bigemina. Among the 10 larval pools negative for B. bigemina, three proceeded from adult females fed on Babesia-negative buffaloes. The other seven pools were from Babesia-positive animals, three from cattle and four from buffalo calves. Babesia infection levels in tick larvae, quantified by qPCR, were similar in female ticks fed on buffalo and bovine calves. We conclude that water buffalo can sustain tick vector populations and support Babesia infection in levels high enough as to be infective for ticks. Our results also validated the hypothesis that adult female ticks fed on buffalo can transmit the pathogens B. bovis and B. bigemina to their offspring. Nevertheless, further laboratory studies are needed to address the question of whether the transovarial transmission of Babesia occurs in the following settings: (1) When adult females are infected previous to the feeding on the buffalo or/and (2) when the adult females acquire the infection while feeding on the buffalo. Full article
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37 pages, 2829 KiB  
Article
Upscaling the Surveillance of Tick-Borne Pathogens in the French Caribbean Islands
by Mathilde Gondard, Sabine Delannoy, Valérie Pinarello, Rosalie Aprelon, Elodie Devillers, Clémence Galon, Jennifer Pradel, Muriel Vayssier-Taussat, Emmanuel Albina and Sara Moutailler
Pathogens 2020, 9(3), 176; https://doi.org/10.3390/pathogens9030176 - 01 Mar 2020
Cited by 13 | Viewed by 3300
Abstract
Despite the high burden of vector-borne disease in (sub)tropical areas, few information are available regarding the diversity of tick and tick-borne pathogens circulating in the Caribbean. Management and control of vector-borne disease require actual epidemiological data to better assess and anticipate the risk [...] Read more.
Despite the high burden of vector-borne disease in (sub)tropical areas, few information are available regarding the diversity of tick and tick-borne pathogens circulating in the Caribbean. Management and control of vector-borne disease require actual epidemiological data to better assess and anticipate the risk of (re)emergence of tick-borne diseases in the region. To simplify and reduce the costs of such large-scale surveys, we implemented a high-throughput microfluidic real-time PCR system suitable for the screening of the main bacterial and parasitic genera involved in tick-borne disease and potentially circulating in the area. We used the new screening tool to perform an exploratory epidemiological study on 132 adult specimens of Amblyomma variegatum and 446 of Rhipicephalus microplus collected in Guadeloupe and Martinique. Not only the system was able to detect the main pathogens of the area—Ehrlichia ruminantium, Rickettsia africae, Anaplasma marginale, Babesia bigemina and Babesia bovis—but the system also provided evidence of unsuspected microorganisms in Caribbean ticks, belonging to the Anaplasma, Ehrlichia, Borrelia and Leishmania genera. Our study demonstrated how high-throughput microfluidic real-time PCR technology can assist large-scale epidemiological studies, providing a rapid overview of tick-borne pathogen and microorganism diversity, and opening up new research perspectives for the epidemiology of tick-borne pathogens. Full article
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22 pages, 463 KiB  
Review
Evaluation of Disease Causality of Rare Ixodes ricinus-Borne Infections in Europe
by Tal Azagi, Dieuwertje Hoornstra, Kristin Kremer, Joppe W. R. Hovius and Hein Sprong
Pathogens 2020, 9(2), 150; https://doi.org/10.3390/pathogens9020150 - 24 Feb 2020
Cited by 37 | Viewed by 4604
Abstract
In Europe, Ixodes ricinus ticks transmit pathogens such as Borrelia burgdorferi sensu lato and tick-borne encephalitis virus (TBEV). In addition, there is evidence for transmission to humans from I. ricinus of Anaplasma phagocytophilum, Babesia divergens, Babesia microti, Babesia venatorum, Borrelia miyamotoi [...] Read more.
In Europe, Ixodes ricinus ticks transmit pathogens such as Borrelia burgdorferi sensu lato and tick-borne encephalitis virus (TBEV). In addition, there is evidence for transmission to humans from I. ricinus of Anaplasma phagocytophilum, Babesia divergens, Babesia microti, Babesia venatorum, Borrelia miyamotoi, Neoehrlichia mikurensis, Rickettsia helvetica and Rickettsia monacensis. However, whether infection with these potential tick-borne pathogens results in human disease has not been fully demonstrated for all of these tick-borne microorganisms. To evaluate the available evidence for a causative relation between infection and disease, the current study analyses European case reports published from 2008 to 2018, supplemented with information derived from epidemiological and experimental studies. The evidence for human disease causality in Europe found in this review appeared to be strongest for A. phagocytophilum and B. divergens. Nonetheless, some knowledge gaps still exist. Importantly, comprehensive evidence for pathogenicity is lacking for the remaining tick-borne microorganisms. Such evidence could be gathered best through prospective studies, for example, studies enrolling patients with a fever after a tick bite, the development of specific new serological tools, isolation of these microorganisms from ticks and patients and propagation in vitro, and through experimental studies. Full article
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