Pathogenesis and Diagnostics of Angiostrongylus vasorum Infection

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

Deadline for manuscript submissions: closed (30 September 2022) | Viewed by 14673

Special Issue Editors


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Guest Editor
Institute of Parasitology, Vetsuisse Faculty, University of Zurich, Winterthurerstr. 266a, CH-8057 Zurich, Switzerland
Interests: veterinary parasitology; cardiopulmonary and intestinal nematodes; diagnostics; epidemiology; control measures; pathogenesis; host-parasite interaction

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Guest Editor
Division of Cardiology, Department for Small Animals, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 260, CH-8057 Zurich, Switzerland
Interests: cardiology; companion animals; pulmonary hypertension; catheter interventions

Special Issue Information

Dear Colleagues,

Discovered in the 19th century in France, Angiostrongylus vasorum is a cardiopulmonary nematode of dogs and wild carnivores and is, therefore, also called “The French heartworm”.

The numerous case reports, prevalence studies and clinical surveys published mainly in the past two decades illustrate, however, the ‘international success’ of this parasite. Adult worms of 1.5-2.5 cm of size reside in the right heart and pulmonary arteries, while their offspring, i.e., first-stage larvae (approx. 365 µm long), cause verminous pneumonia in the definitive canid host. Therefore, canine angiostrongylosis is associated with respiratory distress, but also with bleeding, neurological signs and several other manifestations. This broad range of clinical signs induced by A. vasorum infections has contributed to its attribute of a “great imitator”.

A consequence of the slow but constant establishment of new local hotspots is the risk of misinterpretations and delayed clinical diagnosis of the infection in dogs, particularly in recently discovered endemic areas where disease awareness and the use of appropriate diagnostic procedures are yet not established. Timely diagnosis is, however, important in view of the severe and permanent lung and cardiovascular lesions that may occur. In this context, in addition to copromicroscopic methods detecting the first-stage larvae, serological methods for antigen and antibody detection, as well as biomolecular methods for DNA detection in different substrates, have been developed in order to improve diagnostics for individual animals. Furthermore, diagnostic imaging was shown to be helpful in staging the extent of the lung damage and identifying the potential presence of pulmonary hypertension. Together with single altered laboratory results, these non-pathognomonic findings may be highly indicative for experts in the field.

Despite the major steps forward achieved in diagnostic options, there are still many unresolved key issues that hamper the timely identification of affected animals.

This Special Issue is devoted to collecting original work with the aim of shedding light on some poorly known aspects of this highly fascinating parasite. We focus on diagnostic findings in the clinical and laboratory context and on the pathogenesis of canine angiostrongylosis. The purpose is to unravel questions arising from the available diagnostic options and shed light on some poorly known aspects in the development of the disease.

These aspects are of value in the frame of a) veterinary medicine, in particular for clinical practitioners, and b) parasitology research, by contributing to better understanding of the mechanisms underlying the disease, and therefore advancing potential accompanying therapeutic options.

Prof. Dr. Manuela Schnyder
Prof. Dr. Tony M. Glaus
Guest Editors

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Keywords

  • Canine angiostrongylosis
  • Angiostrongylus vasorum (French Heartworm)
  • Cardiopulmonary nematode
  • Disease awareness
  • Pathogenesis
  • Diagnostics
  • Treatment

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Published Papers (4 papers)

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Research

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13 pages, 4786 KiB  
Article
Angiostrongylus vasorum, Aelurostrongylus abstrusus, Crenosoma vulpis and Troglostrongylus brevior Infections in Native Slug Populations of Bavaria and Baden-Wuerttemberg in Germany
by Lisa Segeritz, Katharina Mareike Westhoff, Roland Schaper, Carlos Hermosilla and Anja Taubert
Pathogens 2022, 11(7), 747; https://doi.org/10.3390/pathogens11070747 - 30 Jun 2022
Cited by 4 | Viewed by 2165
Abstract
Angiostrongylus vasorum, Crenosoma vulpis, Aelurostrongylus abstrusus and Troglostrongylus brevior can cause severe cardiovascular and pulmonary symptoms in companion animals and wildlife. Recently, these nematodes were reported to spread within Europe and South America. The reasons behind this are still unknown, but obligate [...] Read more.
Angiostrongylus vasorum, Crenosoma vulpis, Aelurostrongylus abstrusus and Troglostrongylus brevior can cause severe cardiovascular and pulmonary symptoms in companion animals and wildlife. Recently, these nematodes were reported to spread within Europe and South America. The reasons behind this are still unknown, but obligate gastropod intermediate host populations might play a role. Therefore, lungworm infections in terrestrial slug populations in selected geographic areas of the Federal States of Bavaria and of Baden-Wuerttemberg, Germany, were studied. In total, 517 slugs (462 Arion spp., 51 Deroceras reticulatum, one Limax maximus, and three unknown slug species) were collected in the summer and autumn seasons, artificially digested and microscopically and molecularly analyzed for the presence of metastrongyloid lungworm larvae. Overall, gastropods showed a prevalence of 11.61% (60/517) for A. vasorum, 1.74% (9/517) for A. abstrusus, 0.77% (4/517) for C. vulpis and 0.97% (5/517) for T. brevior infections, respectively. In Obrigheim (Baden-Wuerttemberg), a hyperendemic focus of canine angiostrongylosis was identified. Here, gastropod infection rates rose from 13.60% (17/125) to 62.96% (34/54) within a few months. In total, 25.61% (84/328) of analysed terrestrial gastropods from Baden-Wuerttemberg were positive for metastrongyloids. In contrast, Bavarian gastropods showed a much lower prevalence of 4.76% (9/189). For the first time, the presence of T. brevior was confirmed for Arion spp. in Baden-Wuerttemberg via molecular analyses. Overall, the current data confirm that canine angiostrongylosis occurs in hyperendemic foci in certain geographic areas with high infection rates in intermediate host populations. As a result, the prevalence for a specific region can rise remarkably within a short period of time. Thus, for a better understanding of lungworm epidemiology in Germany and to protect dogs from angiostrongylosis in hyperendemic foci, it seems mandatory to enhance current efforts on Metastrongyloidea-targeted monitoring on a geographical and time span-related level. Full article
(This article belongs to the Special Issue Pathogenesis and Diagnostics of Angiostrongylus vasorum Infection)
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16 pages, 1385 KiB  
Article
Fox Serum Proteomics Analysis Suggests Host-Specific Responses to Angiostrongylus vasorum Infection in Canids
by Nina Gillis-Germitsch, Tobias Kockmann, Christian M. O. Kapel, Stig M. Thamsborg, Pia Webster, Lucienne Tritten and Manuela Schnyder
Pathogens 2021, 10(11), 1513; https://doi.org/10.3390/pathogens10111513 - 19 Nov 2021
Cited by 6 | Viewed by 2618
Abstract
Dogs infected with the cardiopulmonary nematode Angiostrongylus vasorum may suffer from respiratory distress and/or bleeding disorders. Descriptions of clinical signs in foxes are rare, despite high prevalence. To evaluate the impact of infection on coagulation and immune response, serum proteins from eight experimentally [...] Read more.
Dogs infected with the cardiopulmonary nematode Angiostrongylus vasorum may suffer from respiratory distress and/or bleeding disorders. Descriptions of clinical signs in foxes are rare, despite high prevalence. To evaluate the impact of infection on coagulation and immune response, serum proteins from eight experimentally infected foxes before and after inoculation (day 0, 35, 84, 154) were subjected to differential proteomic analyses based on quantitative data and compared to available data from dogs. The number of proteins with differential abundance compared to the uninfected baseline increased with chronicity of infection. Bone marrow proteoglycan, chitinase 3-like protein 1 and pulmonary surfactant-associated protein B were among the most prominently increased proteins. The abundance of several proteins involved in coagulation was decreased. Enriched pathways obtained from both increased and decreased proteins included, among others, “platelet degranulation” and “haemostasis”, and indicated both activation and suppression of coagulation. Qualitative comparison to dog data suggests some parallel serum proteomic alterations. The comparison, however, also indicates that foxes have a more adequate immunopathological response to A. vasorum infection compared to dogs, facilitating persistent infections in foxes. Our findings imply that foxes may be more tolerant to A. vasorum infection, as compared to dogs, reflecting a longer evolutionary host–parasite adaptation in foxes, which constitute a key wildlife reservoir. Full article
(This article belongs to the Special Issue Pathogenesis and Diagnostics of Angiostrongylus vasorum Infection)
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13 pages, 263 KiB  
Article
Coagulation Status in Dogs Naturally Infected with Angiostrongylus vasorum
by Nadja E. Sigrist, Lucienne Tritten, Claudia Kümmerle-Fraune, Natalie Hofer-Inteeworn, Rahel Jud Schefer, Manuela Schnyder and Annette P. N. Kutter
Pathogens 2021, 10(9), 1077; https://doi.org/10.3390/pathogens10091077 - 25 Aug 2021
Cited by 14 | Viewed by 3015
Abstract
Angiostrongylus vasorum infection has been associated with coagulopathies including hyperfibrinolysis. We compared coagulation status including thromboelastometry (ROTEM) parameters in dogs naturally infected with A. vasorum versus healthy dogs to determine clinicopathological parameters associated with bleeding, hypocoagulopathy, and hyperfibrinolysis. Clinical signs, white blood cell [...] Read more.
Angiostrongylus vasorum infection has been associated with coagulopathies including hyperfibrinolysis. We compared coagulation status including thromboelastometry (ROTEM) parameters in dogs naturally infected with A. vasorum versus healthy dogs to determine clinicopathological parameters associated with bleeding, hypocoagulopathy, and hyperfibrinolysis. Clinical signs, white blood cell count, platelet count, hematocrit, plasmatic coagulation tests (PT, aPTT, fibrinogen concentration), D-dimer, and ROTEM S parameters (Ex-tem, In-tem, Fib-tem, Ap-tem) were analysed and compared between bleeding, nonbleeding, and control dogs and between hypo- and normocoagulable animals. Clinical signs of bleeding were present in 6/9 (67%) hypocoagulable and 1/9 (11%) normocoagulable dogs. PT, fibrinogen concentration, and several ROTEM parameters were significantly different between hypocoagulable and normocoagulabe A. vasorum infected dogs. Hyperfibrinolysis was identified in 44% of infected dogs and was significantly more common in bleeding and hypocoagulable dogs. Hyperfibrinolysis was significantly associated with low MCFFib-tem but not with low fibrinogen concentration or increased D-dimers. CFTEx-tem > 248 swas 100% sensitive and 89% specific to predict hyperfibrinolysis. Hyperfibrinolysis, hypocoagulability and bleeding are common in A. vasorum infected dogs. Only Ex-tem and Fib-tem parameters and potentially PT were associated with bleeding or hypocoagulability. Ex-tem analysis enables detection of bleeding, hypocoagulability and hyperfibrinolysis within minutes. Full article
(This article belongs to the Special Issue Pathogenesis and Diagnostics of Angiostrongylus vasorum Infection)

Review

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18 pages, 1816 KiB  
Review
Hemostatic Dysfunction in Dogs Naturally Infected with Angiostrongylus vasorum—A Narrative Review
by Jakob L. Willesen, Rebecca Langhorn and Lise N. Nielsen
Pathogens 2022, 11(2), 249; https://doi.org/10.3390/pathogens11020249 - 14 Feb 2022
Cited by 9 | Viewed by 5630
Abstract
This narrative review aims to describe Angiostrongylus vasorum-induced hemostatic dysfunction of dogs with emphasis on clinical and laboratory findings as well as potential therapeutic strategies for the bleeding patient. Canine angiostrongylosis (CA) is a disease with potentially high morbidity and mortality in [...] Read more.
This narrative review aims to describe Angiostrongylus vasorum-induced hemostatic dysfunction of dogs with emphasis on clinical and laboratory findings as well as potential therapeutic strategies for the bleeding patient. Canine angiostrongylosis (CA) is a disease with potentially high morbidity and mortality in endemic areas and with fatal outcome often associated with either severe respiratory compromise, pulmonary hypertension and right-sided heart failure, or hemostatic dysfunction with severe bleeding. The most common signs of hemorrhage are hematomas, petecchiation, ecchymoses, oral mucosal membrane bleeding and scleral bleeding, while intracranial and pulmonary hemorrhage are among the most severe. The pathophysiological mechanisms underlying hemostatic dysfunction in these patients are presently researched. While the larval effect on platelets remains unknown, the parasite appears to induce dysregulation of hemostatic proteins, with studies suggesting a mixture of pro-coagulant protein consumption and hyperfibrinolysis. Importantly, not all dogs display the same hemostatic abnormalities. Consequently, characterizing the hemostatic state of the individual patient is necessary, but has proven difficult with traditional coagulation tests. Global viscoelastic testing shows promise, but has limited availability in general practice. Treatment of A. vasorum-infected dogs with hemostatic dysfunction relies on anthelmintic treatment as well as therapy directed at the individual dog’s specific hemostatic alterations. Full article
(This article belongs to the Special Issue Pathogenesis and Diagnostics of Angiostrongylus vasorum Infection)
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