Research

14 pages, 3316 KiB

Open AccessArticle

The Zoonotic Angiostrongylus cantonensis and the Veterinary Parasite Aelurostrongylus abstrusus Infecting Terrestrial Gastropods from Urban Areas of Macapá, Brazilian Amazon Region

by Tatiane Alves Barbosa, Silvana Carvalho Thiengo, Monica Ammon Fernandez, Jucicleide Ramos-de-Souza and Suzete Rodrigues Gomes

Pathogens 2024, 13(3), 255; https://doi.org/10.3390/pathogens13030255 - 15 Mar 2024

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Abstract

Metastrongyloidea includes nematodes that parasitize mammals, mainly infecting their respiratory and cardiovascular systems, and are responsible for emerging zoonosis in the world. Terrestrial mollusks are their main intermediate hosts, with few exceptions. Here we present the results of a malacological survey to know [...] Read more.

Metastrongyloidea includes nematodes that parasitize mammals, mainly infecting their respiratory and cardiovascular systems, and are responsible for emerging zoonosis in the world. Terrestrial mollusks are their main intermediate hosts, with few exceptions. Here we present the results of a malacological survey to know the distribution of Angiostrongylus cantonensis in Macapá, Amapá, in the Brazilian Amazon region, after the report of a case of eosinophilic meningitis in 2018. Mollusks were collected in 45 neighborhoods between March 2019 and February 2020. They were identified, parasitologically analyzed, and their nematodes parasites were identified based on the morphology and MT-CO1 sequencing. Infections of An. cantonensis were observed in Achatina fulica, Sarasinula linguaeformis and Subulina octona. These are the first records of the natural infection of the last two species by An. cantonensis in the Brazilian Amazon region. The angiostrongylid Aelurostrongylus abstrusus, which parasitizes cats, was also detected parasitizing A. fulica and Diplosolenodes occidentalis. This is also the first record of the slug D. occidentalis infected by Ae. abstrusus. The highest infection rates were recorded in neighborhoods where the environment conditions favor the proliferation of both mollusks and rodents. The results demonstrate the ample distribution of An. cantonensis in Macapá and the need for surveillance and mollusk vector control in Brazil and other countries. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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10 pages, 705 KiB

Open AccessArticle

Parasite Fauna and Coinfections in Urban Rats Naturally Infected by the Zoonotic Parasite Angiostrongylus cantonensis

by María Teresa Galán-Puchades, Carla Gosálvez, María Trelis, Mercedes Gómez-Samblás, Jennifer Solano-Parada, Antonio Osuna, Sandra Sáez-Durán, Rubén Bueno-Marí and Marius V. Fuentes

Pathogens 2024, 13(1), 28; https://doi.org/10.3390/pathogens13010028 - 27 Dec 2023

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Abstract

When the zoonotic parasite of rodents that can cause human neuroangiostrongyliasis, i.e., Angiostrongylus cantonensis, is found in its natural definitive hosts, it is usually reported in isolation, as if the rat lungworm were the only component of its parasite community. In this study, [...] Read more.

When the zoonotic parasite of rodents that can cause human neuroangiostrongyliasis, i.e., Angiostrongylus cantonensis, is found in its natural definitive hosts, it is usually reported in isolation, as if the rat lungworm were the only component of its parasite community. In this study, we report the coinfections found in rats naturally infected by A. cantonensis in urban populations of Rattus norvegicus and Rattus rattus in Valencia, Spain. In addition to the rat lungworms, which were found in 14 of the 125 rats studied (a prevalence of 11.20%), 18 other parasite species (intestinal and tissular protists, microsporidia and helminths) were found, some of them with high burdens. Fourteen of these nineteen species found are potential zoonotic parasites, namely Blastocystis, Giardia duodenalis, Cryptosporidium spp., Enterocytozoon bieneusi, Encephalitozoon hellem, Toxoplasma gondii, Brachylaima spp., Hydatigera taeniaeformis s.l. larvae, Hymenolepis nana, Hymenolepis diminuta, Angiostrongylus cantonensis, Calodium hepaticum, Gongylonema neoplasticum and Moniliformis moniliformis. The total predominance of coinfected rats as well as their high parasite loads seem to indicate a trend towards parasite tolerance. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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13 pages, 4968 KiB

Open AccessArticle

In the Dawn of an Early Invasion: No Genetic Diversity of Angiostrongylus cantonensis in Ecuador?

by Luis Solórzano Álava, Cesar Bedoya Pilozo, Hilda Hernandez Alvarez, Lazara Rojas Rivera, Misladys Rodriguez Ortega, Jorge Fraga Nodarse, Leandro de Mattos Pereira, Raquel de Oliveira Simões and Roberto do Val Vilela

Pathogens 2023, 12(7), 878; https://doi.org/10.3390/pathogens12070878 - 27 Jun 2023

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Abstract

The nematode Angiostrongylus cantonensis has been reported worldwide. However, some basic questions remain unanswered about A. cantonensis in Ecuador: (1) Was the invasion of A. cantonensis in Ecuador unique, or did it occur in different waves? (2) Was this invasion as [...] Read more.

The nematode Angiostrongylus cantonensis has been reported worldwide. However, some basic questions remain unanswered about A. cantonensis in Ecuador: (1) Was the invasion of A. cantonensis in Ecuador unique, or did it occur in different waves? (2) Was this invasion as recent as historical records suggest? (3) Did this invasion come from other regions of South America or elsewhere? To address these issues, we assessed the genetic diversity of MT-CO1 gene sequences from isolates obtained in 11 of Ecuador’s 24 provinces. Our Bayesian inference phylogenetic tree recovered A. cantonensis as a well-supported monophyletic group. All 11 sequences from Ecuador were identical and identified as AC17a. The haplotype AC17a, found in Ecuador and the USA, formed a cluster with AC17b (USA), AC13 (Thailand), and AC12a-b (Cambodia). Notably, all the samples obtained in Ecuadorian provinces’ different geographic and climatic regions had no genetic difference. Despite the lack of genetic information on A. cantonensis in Latin America, except in Brazil, our finding differs from previous studies by its absence of gene diversity in Ecuador. We concluded that the invasion of A. cantonensis in Ecuador may have occurred: (1) as a one-time event, (2) recently, and (3) from Asia via the USA. Further research should include samples from countries neighboring Ecuador to delve deeper into this. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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16 pages, 1282 KiB

Open AccessArticle

Barriers with Valve Mechanisms Are Predicted to Protect Crops from Slug Carriers of Rat Lungworm Disease

by Genevieve C. Pang, Amy T. Hou, Ryan Tamashiro, Kristin M. Mills and Lorrin W. Pang

Pathogens 2023, 12(6), 847; https://doi.org/10.3390/pathogens12060847 - 19 Jun 2023

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Abstract

Angiostrongyliasis (Rat Lungworm disease) is an emerging parasitic disease caused by the ingestion of gastropods infected with the neurotropic nematode Angiostrongylus cantonensis. The reduction of crop infestation with infected slug carriers may vary widely by protection method. We explored the application of [...] Read more.

Angiostrongyliasis (Rat Lungworm disease) is an emerging parasitic disease caused by the ingestion of gastropods infected with the neurotropic nematode Angiostrongylus cantonensis. The reduction of crop infestation with infected slug carriers may vary widely by protection method. We explored the application of barriers with valve mechanisms, whereby selective directional forces caused a greater number of slugs to exit than enter the protected plot, leading to decreased slug population densities at a steady state. Using field data, we constructed predictive models to estimate slug population densities at a steady state in protected plots with (1) no valve effect, (2) a valve effect, (3) no valve effect with a single breach of the barrier, (4) a valve effect with a single breach of the barrier, (5) a valve effect with a constant breach of the barrier, and (6) a repelling effect. For all scenarios, plots protected using a barrier with a valve effect had consistently lower slug densities at a steady state. Our findings support the use of barriers with valve mechanisms under different conditions, and potentially in combination with other interventions to reduce the contamination of crops by slug carriers of A. cantonensis. Improving barriers extends beyond disease mitigation to economic and cultural impacts on the local farmer and consumer communities. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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16 pages, 13265 KiB

Open AccessArticle

The Global Spread Pattern of Rat Lungworm Based on Mitochondrial Genetics

by Xia Tian, Shen Chen, Lei Duan, Yingjun Qian, Hongmei Li and Shan Lv

Pathogens 2023, 12(6), 788; https://doi.org/10.3390/pathogens12060788 - 31 May 2023

Cited by 1 | Viewed by 1264

Abstract

Eosinophilic meningitis due to rat lungworm, Angiostrongylus cantonensis, is a global public health concern. Human cases and outbreaks have occurred in the new endemic areas, including South America and Spain. The growing genetic data of A. cantonensis provides a unique opportunity to [...] Read more.

Eosinophilic meningitis due to rat lungworm, Angiostrongylus cantonensis, is a global public health concern. Human cases and outbreaks have occurred in the new endemic areas, including South America and Spain. The growing genetic data of A. cantonensis provides a unique opportunity to explore the global spread pattern of the parasite. Eight more mitochondrial (mt) genomes were sequenced by the present study. The phylogeny of A. cantonensis by Bayesian inference showed six clades (I–VI) determined by network analysis. A total of 554 mt genomes or fragments, which represented 1472 specimens of rat lungworms globally, were used in the present study. We characterized the gene types by mapping a variety of mt gene fragments to the known complete mt genomes. Six more clades (I2, II2, III2, V2, VII and VIII) were determined by network analysis in the phylogenies of cox1 and cytb genes. The global distribution of gene types was visualized. It was found that the haplotype diversity of A. cantonensis in Southeast and East Asia was significantly higher than that in other regions. The majority (78/81) of samples beyond Southeast and East Asia belongs to Clade II. The new world showed a higher diversity of Clade II in contrast with the Pacific. We speculate that rat lungworm was introduced from Southeast Asia rather than the Pacific. Therefore, systematic research should be conducted on rat lungworm at a global level in order to reveal the scenarios of spread. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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10 pages, 1024 KiB

Open AccessArticle

Rapid Single-Step Immunochromatographic Assay for Angiostrongylus cantonensis Specific Antigen Detection

by Praphathip Eamsobhana, Anchalee Tungtrongchitr, Darawan Wanachiwanawin, Sudarat Boonyong and Hoi-Sen Yong

Pathogens 2023, 12(6), 762; https://doi.org/10.3390/pathogens12060762 - 25 May 2023

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Abstract

Angiostrongylus cantonensis is the major etiological nematode parasite causing eosinophilic meningitis and/or eosinophilic meningoencephalitis in humans. The rapid global spread of Angiostrongylus cantonensis and the emerging occurrence of the infection have exposed the shortcomings of traditional/conventional diagnostics. This has spurred efforts to develop [...] Read more.

Angiostrongylus cantonensis is the major etiological nematode parasite causing eosinophilic meningitis and/or eosinophilic meningoencephalitis in humans. The rapid global spread of Angiostrongylus cantonensis and the emerging occurrence of the infection have exposed the shortcomings of traditional/conventional diagnostics. This has spurred efforts to develop faster, simpler and more scalable platforms that can be decentralized for point-of-need laboratory testing. By far, the point-of-care immunoassays such as the lateral flow assay (LFA) are the best-placed. In this work, a LFA in the form of an immunochromatographic test device (designated AcAgQuick^Dx), based on the detection of a circulating Angiostrongylus cantonensis-derived antigen, was established using anti-31 kDa Angiostrongylus cantonensis antibody as the capture reagent and anti-Angiostrongylus cantonensis polyclonal antibody as the indicator reagent. The AcAgQuick^Dx was evaluated for its diagnostic potential with a total of 20 cerebrospinal fluids (CSF) and 105 serum samples from patients with angiostrongyliasis and other clinically related parasitic diseases, as well as serum samples from normal healthy subjects. Three of the ten CSF samples from serologically confirmed angiostrongyliasis cases and two of the five suspected cases with negative anti-Angiostrongylus cantonensis antibodies showed a positive AcAgQuick^Dx reaction. Likewise, the AcAgQuick^Dx was able to detect Angiostrongylus cantonensis specific antigens in four serum samples of the 27 serologically confirmed angiostrongyliasis cases. No positive reaction by AcAgQuick^Dx was observed in any of the CSF (n = 5) and serum (n = 43) samples with other parasitic infections, or the normal healthy controls (n = 35). The AcAgQuick^Dx enabled the rapid detection of active/acute Angiostrongylus cantonensis infection. It is easy to use, can be transported at room temperature and does not require refrigeration for long-term stability over a wide range of climate. It can supplement existing diagnostic tests for neuroangiostrongyliasis under clinical or field environments, particularly in remote and resource-poor areas. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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10 pages, 854 KiB

Open AccessArticle

Comparison of Antibody Isotype Response to Angiostrongylus cantonensis in Experimentally Infected Rats (Rattus norvegicus) Using Hawai’i 31 kDa Antigen in an Indirect ELISA

by Argon Steel, Lisa Kaluna, John Jacob and Susan Jarvi

Pathogens 2023, 12(4), 625; https://doi.org/10.3390/pathogens12040625 - 21 Apr 2023

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Abstract

Neuroangiostrongyliasis (NAS) is an emerging tropical disease in humans and some animals which is caused by infection with the parasitic nematode Angiostrongylus cantonensis. It is the leading cause of eosinophilic meningitis worldwide. Diagnoses in humans and susceptible animals are generally presumptive and [...] Read more.

Neuroangiostrongyliasis (NAS) is an emerging tropical disease in humans and some animals which is caused by infection with the parasitic nematode Angiostrongylus cantonensis. It is the leading cause of eosinophilic meningitis worldwide. Diagnoses in humans and susceptible animals are generally presumptive and easily confused with other central nervous system disorders. The 31 kDa antigen is currently the only NAS immunodiagnostic assay that has achieved 100% sensitivity. However, little is known about the humoral immune response against the 31 kDa antigen in NAS infections, which would be critical for widespread adoption of this assay. We used the Hawai’i 31 kDa isolate in an indirect ELISA assay to confirm the presence of immunoglobulin IgG, IgM, IgA, and IgE isotypes in six-week post-infection plasma from lab-reared rats infected with 50 live, third-stage, A. cantonensis larvae isolated from a wild Parmarion martensi semi-slug. Our results confirmed the presence of all four isotypes against the Hawaii 31 kDa isolate, with sensitivity ranging from 22–100%. The IgG isotype showed 100% sensitivity in detecting A. cantonensis infection, which validates the use of IgG indirect ELISA with 31 kDa antigen as an effective immunodiagnostic assay for rats six weeks post-infection. Given each isotype may be present at different times during NAS infections, our data provides preliminary information on the humoral immune response to A. cantonensis infection in lab-reared rats and serves as a baseline for future studies. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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11 pages, 1198 KiB

Open AccessArticle

Successful Removal of Angiostrongylus cantonensis Larvae from the Central Nervous System of Rats 7- and 14-Days Post-Infection Using a Product Containing Moxidectin, Sarolaner and Pyrantel Embonate (Simparica Trio™) in Experimental Infections

by Michaela Henry, Richard Malik, Jan Šlapeta and Rogan Lee

Pathogens 2023, 12(2), 305; https://doi.org/10.3390/pathogens12020305 - 12 Feb 2023

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Abstract

Angiostrongylus cantonensis is a nematode with an indirect lifecycle, using molluscs as intermediate hosts. Rats are the definitive host. By administering a suitable anthelmintic, at an appropriate interval, the risk of clinical neuroangiostrongyliasis occurring in paratenic hosts (e.g., dogs, man) can be eliminated. [...] Read more.

Angiostrongylus cantonensis is a nematode with an indirect lifecycle, using molluscs as intermediate hosts. Rats are the definitive host. By administering a suitable anthelmintic, at an appropriate interval, the risk of clinical neuroangiostrongyliasis occurring in paratenic hosts (e.g., dogs, man) can be eliminated. We wanted to determine if infective larvae (L3) of A. cantonensis can be safely killed during their migration through the central nervous system (CNS) by oral administration of an anthelmintic combination containing moxidectin (480 µg/kg, Simparica Trio™; M-S-P), thereby preventing patent infections in rats. Eighteen rats were used: ten received oral M-S-P every four weeks; eight rats were used as controls. Rats were initially given M-S-P as a chew to eat, but an acquired food aversion meant that subsequent doses were given by orogastric lavage. All 18 rats were challenged once or twice with approximately 30 L3 A. cantonensis larvae via orogastric lavage. Infection status was determined by faecal analysis using the Baermann technique and necropsy examination of the heart, pulmonary arteries and lungs. Eight out of ten rats dosed with M-S-P had zero lungworms at necropsy; a single female worm was detected in each of the remaining two rats. No treated rats had L1 larvae in faeces. In contrast, all eight controls were infected with patent infections, with a median of 14.5 worms per rat detected at necropsy. The difference in infection rates was significant (two tailed Fishers Exact; p = 0.0011). Moxidectin given orally once every month killed migrating larvae before they reached the pulmonary arteries in 80% of treated rats, while in 20%, only a single female worm was present. Considering the short half-life of moxidectin in the rat, it is likely that the effectiveness of moxidectin is due to larvicidal action on migrating L3, L4 and L5 larvae in the brain parenchyma or subarachnoid space, either 7 days (L3/L4 in cerebrum and spinal cord) or 14 days (L4/L5 in cerebrum and subarachnoid space) after inoculation. This study is a prelude for future research to determine if monthly moxidectin administration orally as M-S-P could prevent symptomatic neuroangiostrongyliasis in dogs. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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Review

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21 pages, 1445 KiB

Open AccessEditor’s ChoiceReview

An Overview of Angiostrongylus cantonensis (Nematoda: Angiostrongylidae), an Emerging Cause of Human Angiostrongylosis on the Indian Subcontinent

by Divakaran Pandian, Tomáš Najer and David Modrý

Pathogens 2023, 12(6), 851; https://doi.org/10.3390/pathogens12060851 - 20 Jun 2023

Cited by 3 | Viewed by 3572

Abstract

Human angiostrongylosis is an emerging zoonosis caused by the larvae of three species of metastrongyloid nematodes of the genus Angiostrongylus, with Angiostrongylus cantonensis (Chen, 1935) being dominant across the world. Its obligatory heteroxenous life cycle includes rats as definitive hosts, mollusks as intermediate [...] Read more.

Human angiostrongylosis is an emerging zoonosis caused by the larvae of three species of metastrongyloid nematodes of the genus Angiostrongylus, with Angiostrongylus cantonensis (Chen, 1935) being dominant across the world. Its obligatory heteroxenous life cycle includes rats as definitive hosts, mollusks as intermediate hosts, and amphibians and reptiles as paratenic hosts. In humans, the infection manifests as Angiostrongylus eosinophilic meningitis (AEM) or ocular form. Since there is no comprehensive study on the disease in the Indian subcontinent, our study aims at the growing incidence of angiostrongylosis in humans, alongside its clinical course and possible causes. A systematic literature search revealed 28 reports of 45 human cases from 1966 to 2022; eosinophilic meningitis accounted for 33 cases (75.5%), 12 cases were reported as ocular, 1 case was combined, and 1 case was unspecified. The presumed source of infection was reported in 5 cases only. Importantly, 22 AEM patients reported a history of eating raw monitor lizard (Varanus spp.) tissues in the past. As apex predators, monitor lizards accumulate high numbers of L3 responsible for acute illness in humans. For ocular cases, the source was not identified. Most cases were diagnosed based on nematode findings and clinical pathology (primarily eosinophilia in the cerebrospinal fluid). Only two cases were confirmed to be A. cantonensis, one by immunoblot and the other by q-PCR. Cases of angiostrongylosis have been reported in Delhi, Karnataka, Kerala, Maharashtra, Madhya Pradesh, Puducherry, Telangana, and West Bengal. With a population of more than 1.4 billion, India is one of the least studied areas for A. cantonensis. It is likely that many cases remain undetected/unreported. Since most cases have been reported from the state of Kerala, further research may focus on this region. Gastropods, amphibians, and reptiles are commonly consumed in India; however, typical preparation methods involve cooking, which kills the nematode larvae. In addition to studying rodent and mollusk hosts, monitor lizards can be used as effective sentinels. Sequence data are urgently needed to answer the question of the identity of Angiostrongylus-like metastrongylid nematodes isolated from all types of hosts. DNA-based diagnostic methods such as q-PCR and LAMP should be included in clinical diagnosis of suspected cases and in studies of genetic diversity and species identity of nematodes tentatively identified as A. cantonensis. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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Other

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8 pages, 651 KiB

Open AccessViewpoint

Neuroangiostrongyliasis: Updated Provisional Guidelines for Diagnosis and Case Definitions

by Carlos Graeff-Teixeira, Kittisak Sawanyawisuth, Shan Lv, William Sears, Zhaily González Rodríguez, Hilda Hernández Álvarez, Pedro Casanova Arias, Leticia Karolini Walger Schultz, Alicia Rojas, John Jacob, Susan Jarvi and Kenton Kramer

Pathogens 2023, 12(4), 624; https://doi.org/10.3390/pathogens12040624 - 20 Apr 2023

Cited by 1 | Viewed by 1672

Abstract

Angiostrongylus cantonensis is the main causative agent for eosinophilic meningoencephalitis in humans. Larvae are rarely found in the cerebral spinal fluid (CSF). Consequently, serology and DNA detection represent important diagnostic tools. However, interpretation of the results obtained from these tools requires that more [...] Read more.

Angiostrongylus cantonensis is the main causative agent for eosinophilic meningoencephalitis in humans. Larvae are rarely found in the cerebral spinal fluid (CSF). Consequently, serology and DNA detection represent important diagnostic tools. However, interpretation of the results obtained from these tools requires that more extensive accuracy studies be conducted. The aim of the present study is to update guidelines for diagnosis and case definitions of neuroangiostrongyliasis (NA) as provided by a working group of a recently established International Network on Angiostrongyliasis. A literature review, a discussion regarding criteria and diagnostic categories, recommendations issued by health authorities in China and an expert panel in Hawaii (USA), and the experience of Thailand were considered. Classification of NA cases and corresponding criteria are proposed as follows: minor (exposure history, positive serology, and blood eosinophilia); major (headache or other neurological signs or symptoms, CSF eosinophilia); and confirmatory (parasite detection in tissues, ocular chambers, or CSF, or DNA detection by PCR and sequencing). In addition, diagnostic categories or suspected, probable, and confirmatory are proposed. Updated guidelines should improve clinical study design, epidemiological surveillance, and the proper characterization of biological samples. Moreover, the latter will further facilitate accuracy studies of diagnostic tools for NA to provide better detection and treatment. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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6 pages, 235 KiB

Open AccessPerspective

Management of Rat Lungworm Disease (Neuroangiostrongyliasis) Using Anthelmintics: Recent Updates and Recommendations

by John Jacob, Argon Steel, Kathleen Howe and Susan Jarvi

Pathogens 2023, 12(1), 23; https://doi.org/10.3390/pathogens12010023 - 23 Dec 2022

Cited by 1 | Viewed by 1673

Abstract

While there have been legitimate concerns in the past regarding the use of anthelmintics for the management of neuroangiostrongyliasis (rat lungworm disease), recent studies demonstrate that they can be considered safe and efficacious, particularly albendazole, which is regarded as the choice anthelmintic for [...] Read more.

While there have been legitimate concerns in the past regarding the use of anthelmintics for the management of neuroangiostrongyliasis (rat lungworm disease), recent studies demonstrate that they can be considered safe and efficacious, particularly albendazole, which is regarded as the choice anthelmintic for its management. However, physician hesitancy to prescribe, as well as problems of availability persist, at least in Hawaii, which is considered the epicenter of this disease in the US. As a result, many patients suffer a diminished quality of life or even death. Here, we discuss recent studies that provide insights into new treatments and preventative interventions, which can be more rigorously used for the management of neuroangiostrongyliasis. In summary, results from recent studies suggest that albendazole and avermectins are beneficial for post-exposure management, pyrantel pamoate is beneficial as a post-exposure prophylactic, and levamisole is deserving of further study for the treatment of neuroangiostrongyliasis. Full article

(This article belongs to the Special Issue Rat Lungworm Disease)

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