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Ticks & Piroplasms: Updates and Emerging Challenges

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A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Ticks".

Deadline for manuscript submissions: closed (31 December 2023) | Viewed by 22921

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Special Issue Editors

Dr. Ana Domingos

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Guest Editor

Global Health and Tropical Medicine, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisboa, Portugal
Interests: tick and TBP control; epidemiology; tick–host–pathogen interactions

Dr. Sandra Antunes

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Guest Editor

Global Health and Tropical Medicine, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisboa, Portugal
Interests: vectors and vector borne diseases; ticks; pathogens; Babesia sp.; tick–pathogen interactions

Special Issue Information

Dear Colleagues,

Under the phylum Apicomplexa, the order Piroplasmida includes the genera Babesia, Theileria and Cytauxzoon, which comprise intracellular organisms with intricate life cycles, involving asexual multiplication within a vertebrate host and sexual multiplication followed by sporozoite formation in an arthropod vector, namely, ticks.

These parasites can infect a wide range of vertebrate hosts and share many similarities but also distinctive characteristics, as the pre-erythrocytic life stage in leukocytes found in Theileria sp. and Cytauxzoon sp. but not in Babesia sp. In particular, the disease syndromes “babesiosis” and “theileriosis” are globally recognized due to their extensive prevalence, intrinsically connected to vector distribution, and impact on animal health. The ability to infect humans is restricted to a few number of Babesia species; however, with an alarming rise of cases, particularly in North America, human babesiosis is considered an emerging zoonosis. Such facts allied with the economic losses in husbandry fosters the need to develop and implement effective control strategies and promote global health.

Studies on these two piroplasmids have revealed extraordinary features related to their biology and dynamics within their host cells. Still, much remains to be explored with the wake of omics technologies. Moreover, most of the related research has been focusing on mammal-infecting stages of Babesia and Theileria, neglecting their linkage to ticks. Uncovering the tied interactions occurring at both vector and vertebrate host interface, as well as continuous epidemo-surveillance, are key to the pursuit of disease eradication.

This Special Issue aims to gather updates on current knowledge and beyond, under the thematic of ticks and piroplasms. We encourage the submission of not only research articles or short communications, presenting new data and using different methodologies, but also reviews of the most interesting achievements under this topic. Opinion articles on tick and piroplamids, control measures or programs are also welcome. We are sure that this issue will contribute to a better understanding of the complex tick–piroplasm–host relationship and bring forward innovative solutions to alleviate the negative effects imposed by such association.

Dr. Ana Domingos
Dr. Sandra Antunes
Guest Editors

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Keywords

Babesia sp.
Theileria sp.
Pathogen–host cell interactions
Epidemiology
Public health
Disease control

Published Papers (9 papers)

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Research

Jump to: Review

12 pages, 1186 KiB

Open AccessEditor’s ChoiceArticle

A U.S. Isolate of Theileria orientalis Ikeda Is Not Transstadially Transmitted to Cattle by Rhipicephalus microplus

by Cynthia K. Onzere, David R. Herndon, Amany Hassan, Kennan Oyen, Karen C. Poh, Glen A. Scoles and Lindsay M. Fry

Pathogens 2023, 12(4), 559; https://doi.org/10.3390/pathogens12040559 - 05 Apr 2023

Cited by 4 | Viewed by 2242

Abstract

Theileria orientalis Ikeda has caused an epidemic of bovine anemia and abortion across several U.S. states. This apicomplexan hemoparasite is transmitted by Haemaphysalis longicornis ticks; however, it is unknown if other North American ticks are competent vectors. Since the disease movement is largely determined by the host tick range(s), the prediction of the T. orientalis spread among U.S. cattle populations requires determination of additional competent tick vectors. Although Rhipicephalus microplus has mostly been eradicated from the U.S., outbreaks in populations occur frequently, and the U.S. remains at risk for reintroduction. Since R. microplus is a vector of Theileria equi and T. orientalis DNA has been detected in R. microplus, the goal of this study was to determine whether R. microplus is a competent vector of T. orientalis. Larval R. microplus were applied to a splenectomized, T. orientalis Ikeda-infected calf for parasite acquisition, removed as molted adults, and applied to two T. orientalis naïve, splenectomized calves for transmission. After 60 days, the naïve calves remained negative for T. orientalis by PCR and cytology. Additionally, T. orientalis was not detected in the salivary glands or larval progeny of acquisition-fed adults. These data suggest that R. microplus is not a competent vector of the U.S. T. orientalis Ikeda isolate. Full article

(This article belongs to the Special Issue Ticks & Piroplasms: Updates and Emerging Challenges)

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6 pages, 432 KiB

Open AccessCommunication

Detection of Babesia conradae in Coyotes (Canis latrans) and Coyote-Hunting Greyhound Dogs (Canis familiaris)

by Haley Furman and Ruth C. Scimeca

Pathogens 2023, 12(4), 528; https://doi.org/10.3390/pathogens12040528 - 29 Mar 2023

Viewed by 1368

Abstract

Babesia conradae is a small piroplasm previously detected in coyote-hunting Greyhound dogs in California and Oklahoma. In dogs, B. conradae causes clinical signs similar to other tick-borne illnesses, and if not treated it can lead to acute kidney injury and other life-threating complications. To date, the life cycle of this apicomplexan parasite has not been fully described, but suggestions of direct contact or tick transmission have been proposed. The purpose of this study was to test coyote tissue samples from coyotes hunted by Greyhound dogs with a history of B. conradae infection to determine if this parasite is present in the coyote population in Northwestern Oklahoma. The analyzed tissue samples included liver, lung and tongue samples collected by hunters. DNA was isolated from these tissues and assessed by RT-PCR of the 18S rRNA and PCR of the COX1 genes for B. conradae. A total of 66 dogs and 38 coyotes were tested, and the results demonstrated the presence of B. conradae DNA in 21 dogs (31.8%) and 4 coyotes (10.5%). These results indicate that B. conradae is present in the dog and coyote population from the same area and that direct contact with coyotes may increase the risk of infection in dogs. Further studies are required to test possible modes of transmission, including direct bite, tick or vertical transmission. Full article

(This article belongs to the Special Issue Ticks & Piroplasms: Updates and Emerging Challenges)

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17 pages, 1582 KiB

Open AccessArticle

Spherical Body Protein 4 from Babesia bigemina: A Novel Gene That Contains Conserved B-Cell Epitopes and Induces Cross-Reactive Neutralizing Antibodies in Babesia ovata

by Juan Mosqueda, Diego Josimar Hernandez-Silva, Massaro W. Ueti, Adolfo Cruz-Reséndiz, Ricardo Marquez-Cervantez, Uriel Mauricio Valdez-Espinoza, Minh-Anh Dang-Trinh, Thu-Thuy Nguyen, Minerva Camacho-Nuez, Miguel Angel Mercado-Uriostegui, Gabriela Aguilar-Tipacamú, Juan Alberto Ramos-Aragon, Ruben Hernandez-Ortiz, Shin-ichiro Kawazu and Ikuo Igarashi

Pathogens 2023, 12(3), 495; https://doi.org/10.3390/pathogens12030495 - 22 Mar 2023

Cited by 1 | Viewed by 1679

Abstract

Bovine babesiosis is a tick-transmitted disease caused by intraerythrocytic protozoan parasites of the genus Babesia. Its main causative agents in the Americas are Babesia bigemina and Babesia bovis, while Babesia ovata affects cattle in Asia. All Babesia species secrete proteins stored in organelles of the apical complex, which are involved in all steps of the invasion process of vertebrate host cells. Unlike other apicomplexans, which have dense granules, babesia parasites instead have large, round intracellular organelles called spherical bodies. Evidence suggests that proteins from these organelles are released during the process of invading red blood cells, where spherical body proteins (SBPs) play an important role in cytoskeleton reorganization. In this study, we characterized the gene that encodes SBP4 in B. bigemina. This gene is transcribed and expressed in the erythrocytic stages of B. bigemina. The sbp4 gene consists of 834 nucleotides without introns that encode a protein of 277 amino acids. In silico analysis predicted a signal peptide that is cleaved at residue 20, producing a 28.88-kDa protein. The presence of a signal peptide and the absence of transmembrane domains suggest that this protein is secreted. Importantly, when cattle were immunized with recombinant B. bigemina SBP4, antibodies identified B. bigemina and B. ovata merozoites according to confocal microscopy observations and were able to neutralize parasite multiplication in vitro for both species. Four peptides with predicted B-cell epitopes were identified to be conserved in 17 different isolates from six countries. Compared with the pre-immunization sera, antibodies against these conserved peptides reduced parasite invasion in vitro by 57%, 44%, 42%, and 38% for peptides 1, 2, 3, and 4, respectively (p < 0.05). Moreover, sera from cattle infected with B. bigemina cattle contained antibodies that recognized the individual peptides. All these results support the concept of spb4 as a new gene in B. bigemina that should be considered a candidate for a vaccine to control bovine babesiosis. Full article

(This article belongs to the Special Issue Ticks & Piroplasms: Updates and Emerging Challenges)

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14 pages, 3118 KiB

Open AccessArticle

Discovery of a Novel Species Infecting Goats: Morphological and Molecular Characterization of Babesia aktasi n. sp.

by Sezayi Ozubek, Mehmet Can Ulucesme and Munir Aktas

Pathogens 2023, 12(1), 113; https://doi.org/10.3390/pathogens12010113 - 10 Jan 2023

Cited by 4 | Viewed by 2441

Abstract

A novel Babesia sp. infecting goats was discovered based on the molecular findings obtained in the current study, which was conducted in the Mediterranean region of Türkiye. The goal of this study was to isolate this species of Babesia (Babesia sp.) infecting goats in vivo and to assess the genetic and morphological characterization of the parasite. To identify the animal naturally infected with Babesia sp. and isolate the parasite from this animal, field studies were conducted first, and genomic DNA were extracted from blood samples taken from goats (n = 50). The Theileria, Babesia, and Anaplasma species were identified using a nested PCR-based reverse line blotting (RLB) method. The study included one goat that was determined to be infected with Babesia sp. (single infection) in RLB for in vivo isolation. A blood smear was prepared to examine the parasite’s morphology, but it was found to be negative microscopically. Following that, a splenectomy operation (to suppress the immune system) was performed to make the parasites visible microscopically in this animal. Parasitemia began after splenectomy, and the maximum parasitemia was determined to be 1.9%. The goat displayed no significant symptoms other than fever, loss of appetite, and depression. During a period when parasitemia was high, blood from this goat was inoculated into another splenectomized goat (Theileria-Babesia-Anaplasma-Mycoplasma spp. free). On the third day of inoculation, 10% parasitemia with high fever was detected in the goat, and on the fourth day, the goat was humanely euthanized due to severe acute babesiosis symptoms. Except for mild subcutaneous jaundice, no lesions were discovered during the necropsy. According to the microscopic measurement results, ring, double pyriform, spectacle-frame-like, and line forms were observed, and it was observed to be between 1.0–2.5 µm (1.38 ± 0.17 to 0.7 ± 0.21-all forms). A phylogenetic analysis and sequence comparison using the 18S rRNA and cox1 genes revealed that this species is distinct from the small ruminant Babesia species (18S rRNA 92–94%, cox1 79–80%) and has the highest similarity to Babesia sp. deer, which has been reported in deer. Furthermore, it was determined to resemble B. venatorum, B. divergens, Babesia sp. FR1 and Babesia sp. MO1 species, all of which are zoonotic. Additional research is needed to clarify the clinical status of this parasite in goats and other hosts (mountain goat, sheep, calf). Full article

(This article belongs to the Special Issue Ticks & Piroplasms: Updates and Emerging Challenges)

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13 pages, 1977 KiB

Open AccessArticle

Differential Expression of Immune Genes in the Rhipicephalus microplus Gut in Response to Theileria equi Infection

by Patrícia Gonzaga Paulino, Maristela Peckle, Leo Paulis Mendonça, Carlos Luiz Massard, Sandra Antunes, Joana Couto, Ana Domingos, Daniel da Silva Guedes Junior, Alejandro Cabezas-Cruz and Huarrisson Azevedo Santos

Pathogens 2022, 11(12), 1478; https://doi.org/10.3390/pathogens11121478 - 06 Dec 2022

Viewed by 2324

Abstract

Rhipicephalus microplus is the only tick species known to serve as a biological vector of Theileria equi for horses and other equids in Brazil. The protozoan T. equi is one of the causal agents of equine piroplasmosis, a major threat in horse breeding systems. Vector competence is closely linked to the pathogens’ ability to evade tick defense mechanisms. However, knowledge of tick immune response against infections by hemoparasites of the Theileria genus is scarce. In the present study, the expression of genes involved in immune signaling pathways of R. microplus adults’ guts when challenged with a high or low parasitic load of T. equi was evaluated. This research demonstrates divergences in the immune gene expression pattern linked to T. equi infection in R. microplus since the Toll, IMD, and JNK signaling pathways were transcriptionally repressed in the guts of adult ticks infected with T. equi. Moreover, the results showed that different infectious doses of T. equi induce differential gene expression of key components of immune signaling cascades in R. microplus gut, suggesting a link between the intensity of infection and the activation of tick immunity response. The present study adds knowledge to elucidate the gut immune signaling response of R. microplus to T. equi infection. In addition, the generated data can serve as a basis for further investigations to develop strategies for controlling and preventing equine piroplasmosis. Full article

(This article belongs to the Special Issue Ticks & Piroplasms: Updates and Emerging Challenges)

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14 pages, 2329 KiB

Open AccessCommunication

First Molecular Identification of Babesia, Theileria, and Anaplasma in Goats from the Philippines

by Eloiza May Galon, Rochelle Haidee Ybañez, Adrian Miki Macalanda, Giemelene Rose Estabillo, Margaret Therese Rose Montano, Marielle Danise Veedor, Anatolio Garvida, Ralph Joselle Fabon, Mary Ruth Callanta, Kim Joseph Labutong, Maria Agnes Tumwebaze, Benedicto Byamukama, Shengwei Ji, Iqra Zafar, Adrian Ybañez and Xuenan Xuan

Pathogens 2022, 11(10), 1109; https://doi.org/10.3390/pathogens11101109 - 27 Sep 2022

Cited by 3 | Viewed by 2771

Abstract

Goats are key livestock animals and goat raising is an income-generating venture for smallholder farmers, supporting agricultural development in many parts of the world. However, goat production is often limited by various factors, such as tick-borne diseases. Goat piroplasmosis is a disease caused by apicomplexan parasites Babesia spp. and Theileria spp., while anaplasmosis is caused by bacterial Anaplasma spp. In the Philippines, the presence of Babesia, Theileria, and Anaplasma has not been reported in goats. In this study, DNA obtained from goats were molecularly screened for Babesia/Theileria and Anaplasma. Of 396, 77.02% (305/396) and 38.64% (153/396) were positive for piroplasma and Anaplasma using PCR assays targeting the 18S rRNA and 16S rRNA genes, respectively. Similarly, Babesia ovis was detected in six samples (1.52%). Representative Babesia/Theileria sequences shared 89.97–97.74% identity with each other and were most closely related to T. orientalis, T. annulata, and Theileria spp. Meanwhile, Anaplasma 16SrRNA sequences were related to A. odocoilei, A. platys, and A. phagocytophilum. This is the first molecular identification of B. ovis, Theileria spp., and Anaplasma spp. in goats from the Philippines. Full article

(This article belongs to the Special Issue Ticks & Piroplasms: Updates and Emerging Challenges)

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12 pages, 1320 KiB

Open AccessArticle

Spatial and Temporal Circulation of Babesia caballi and Theileria equi in France Based on Seven Years of Serological Data

by Clémence Nadal, Maud Marsot, Gaël Le Metayer, Pascal Boireau, Jacques Guillot and Sarah I. Bonnet

Pathogens 2022, 11(2), 227; https://doi.org/10.3390/pathogens11020227 - 09 Feb 2022

Cited by 2 | Viewed by 1981

Abstract

Caused by two blood parasites, Babesia caballi and Theileria equi, equine piroplasmosis is a tick-borne disease that poses major health and economic issues for the equine industry. Our objective was to gain insight into the spatio-temporal variations of parasite circulation in France, where the disease is known to be enzootic, but has been the subject of few studies. Seroprevalence was assessed for each parasite thanks to 16,127 equine sera obtained between 1997 and 2003 from all over France and analysed through complement fixation tests. Results indicated that 13.2% (5–27% depending on the region) of horses were seropositive for T. equi and 9.5% (3–25%) for B. caballi. Regardless of the year, horses from the southern regions of France were the most affected by B. caballi or T. equi infection, while the proportion of horses having antibodies against T. equi increased over time. These results highlight the heterogeneity of the circulation of both piroplasms, which may be linked with ecological diversity and vector distribution. Our data provide baseline information regarding the sero-epidemiology of B. caballi and T. equi infection in horses in France, making it now possible to select regions for future studies on risk factors, and design and implement effective targeted measures against equine piroplasms. Full article

(This article belongs to the Special Issue Ticks & Piroplasms: Updates and Emerging Challenges)

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Review

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23 pages, 1465 KiB

Open AccessReview

The Diverse Pathogenicity of Various Babesia Parasite Species That Infect Dogs

by Andrew L. Leisewitz, Vladimir Mrljak, Jonathan D. Dear and Adam Birkenheuer

Pathogens 2023, 12(12), 1437; https://doi.org/10.3390/pathogens12121437 - 11 Dec 2023

Cited by 1 | Viewed by 2187

Abstract

Babesia species infect a very wide range of mammal hosts across the globe, and zoonotic infections are of growing concern. Several species of the Babesia genus infect dogs, and some of these cause significant morbidity and mortality. The Apicomplexan parasite resides within the red cell and infections result in direct damage to the host through intra- and extravascular hemolysis. An exuberant inflammatory response by the host to some species of Babesia parasites also results in significant collateral damage to the host. Canine infections have been the subject of many studies as the well-being of these companion animals is increasingly threatened by the spread of tick vectors and an increasingly mobile dog population. There are currently no widely available and effective vaccines, and effective treatment can be challenging. Understanding disease pathogenesis underlies the development of new treatments. The varying pathogenicity of the various Babesia parasite species that infect dogs offers an opportunity to explore the molecular basis for the wide range of diseases caused by infection with this parasite genus. In this review, we focus on what has been reported about the clinical presentation of Babesia-infected dogs in an attempt to compare the severity of disease caused by different Babesia species. Full article

(This article belongs to the Special Issue Ticks & Piroplasms: Updates and Emerging Challenges)

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19 pages, 5205 KiB

Open AccessReview

Cytauxzoon felis: An Overview

by Yvonne M. Wikander and Kathryn E. Reif

Pathogens 2023, 12(1), 133; https://doi.org/10.3390/pathogens12010133 - 13 Jan 2023

Cited by 4 | Viewed by 4465

Abstract

Cytauxzoon felis is a tick-transmitted, obligate, hemoprotozoal, piroplasmid pathogen of felids and the causative agent of cytauxzoonosis. It has a complex life cycle which includes a tick as its definitive host and a felid as its intermediate host. Since its first description in 1976, C. felis infections of felids have been reported in several southeastern and south-central U.S. states, overlapping with the ranges of its two known biological vectors, Amblyomma americanum (Lone star tick) and Dermacentor variabilis (American dog tick). Infected felids demonstrate disease as either an acute, often-fatal, infection, or a subclinical carrier infection. To develop effective C. felis transmission control strategies, the incidence of acute cytauxzoonosis, patient risk factors, the role of domestic cat carriers, and ecological variabilities need to be investigated further. Of equal importance is communicating these strategies for high-risk cat populations, including recommending year-round use of an acaricide product for all cats that spend any time outdoors. More studies are needed to further identify factors affecting C. felis and other Cytauxzoon spp. infection, transmission, disease progression, and treatment options and outcomes within the U.S. and globally. Here we provide an overview of C. felis highlighting its lifecycle within its definitive host, transmission to its intermediate host, symptoms and signs providing evidence of transmission, definitive diagnosis, current treatment and prevention strategies, and future considerations regarding this condition. Full article

(This article belongs to the Special Issue Ticks & Piroplasms: Updates and Emerging Challenges)

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