Efficacy of afoxolaner (NexGard®) in preventing the transmission of <i>Leishmania infantum</i> and <i>Dirofilaria immitis</i> to sheltered dogs in a highly endemic area

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Abstract

Background

Leishmania infantum and Dirofilaria immitis are among the most important canine vector-borne pathogens (CVBPs) of zoonotic concern in Europe. In endemic areas for both of these CVBPs, the use of systemic ectoparasiticides, such as afoxolaner (NexGard®; Boehringer Ingelheim Animal Health), may have the potential for controlling these infections. The aim of this study was to assess, for the first time, the insecticidal efficacy of NexGard® in decreasing the transmission of D. immitis and L. infantum to sheltered dogs living in a hyperendemic area, compared to the year before treatment, as well as its impact on the abundance of mosquito and sand fly populations.

Methods

All dogs ( n = 179) enrolled in the study were divided into two groups based on their infection status at enrollment: a non-infected group (G1) and an infected group (G2; infected with D. immitis, L. infantum or both). The study was conducted from March 2020 to March 2021. In order to exclude all animals infected with L. infantum and D. immitis before March 2020 (sampling time: T0), dogs in G1 were sampled in June (T1; i.e. T0 + 90 days) and in October 2020 (T2; i.e. T0 + 210 days). From March to September 2020, all animals (G1 and G2) were weighed and treated monthly with NexGard®. Animals in G1 were tested for the last time in March 2021 (T3; i.e. T0 + 330 days) for assessing post-treatment incidence rate of infection and prevention efficacy.

Results

The post-treatment incidence of D. immitis was 3.7% (1/27; 95% confidence interval [CI]: 0.2–18.1) and that of L. infantum was 3.6% (3/83; 95% CI: 1.0–10.1). Considering the annual incidence in 2019 and 2020, the protective efficacy against D. immitis and L. infantum infections was 94.2 and 64%, respectively. Of the female mosquitoes collected ( n = 146), only one pool out of 50 tested positive for D. immitis DNA, whereas out of 1252 female Sergentomya minuta specimens collected, only four tested positive for L. infantum (0.3%).

Conclusions

Afoxolaner is efficacious in decreasing the rate of transmission of both D. immitis and L. infantum; however, comparison of the pre- and post-treatment period demonstrated that there was a significant difference only in the seasonal incidences of D. immitis infection. Preventive measures are recommended throughout the year in endemic areas to reduce the risk of pathogen transmission to animals and humans.

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Most cited references 43

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Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern.

M Maroli, M. D. Feliciangeli, L Bichaud … (2013)

Phlebotomine sandflies transmit pathogens that affect humans and animals worldwide. We review the roles of phlebotomines in the spreading of leishmaniases, sandfly fever, summer meningitis, vesicular stomatitis, Chandipura virus encephalitis and Carrión's disease. Among over 800 species of sandfly recorded, 98 are proven or suspected vectors of human leishmaniases; these include 42 Phlebotomus species in the Old World and 56 Lutzomyia species in the New World (all: Diptera: Psychodidae). Based on incrimination criteria, we provide an updated list of proven or suspected vector species by endemic country where data are available. Increases in sandfly diffusion and density resulting from increases in breeding sites and blood sources, and the interruption of vector control activities contribute to the spreading of leishmaniasis in the settings of human migration, deforestation, urbanization and conflict. In addition, climatic changes can be expected to affect the density and dispersion of sandflies. Phlebovirus infections and diseases are present in large areas of the Old World, especially in the Mediterranean subregion, in which virus diversity has proven to be higher than initially suspected. Vesiculovirus diseases are important to livestock and humans in the southeastern U.S.A. and Latin America, and represent emerging human threats in parts of India. Carrión's disease, formerly restricted to regions of elevated altitude in Peru, Ecuador and Colombia, has shown recent expansion to non-endemic areas of the Amazon basin. © 2012 The Authors. Medical and Veterinary Entomology © 2012 The Royal Entomological Society.

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Dirofilariasis represents a zoonotic mosaic, which includes two main filarial species (Dirofilaria immitis and D. repens) that have adapted to canine, feline, and human hosts with distinct biological and clinical implications. At the same time, both D. immitis and D. repens are themselves hosts to symbiotic bacteria of the genus Wolbachia, the study of which has resulted in a profound shift in the understanding of filarial biology, the mechanisms of the pathologies that they produce in their hosts, and issues related to dirofilariasis treatment. Moreover, because dirofilariasis is a vector-borne transmitted disease, their distribution and infection rates have undergone significant modifications influenced by global climate change. Despite advances in our knowledge of D. immitis and D. repens and the pathologies that they inflict on different hosts, there are still many unknown aspects of dirofilariasis. This review is focused on human and animal dirofilariasis, including the basic morphology, biology, protein composition, and metabolism of Dirofilaria species; the climate and human behavioral factors that influence distribution dynamics; the disease pathology; the host-parasite relationship; the mechanisms involved in parasite survival; the immune response and pathogenesis; and the clinical management of human and animal infections.

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The role of dogs as reservoirs of Leishmania parasites, with emphasis on Leishmania (Leishmania) infantum and Leishmania (Viannia) braziliensis.

Filipe Dantas-Torres (2007)

Leishmania parasites cause a group of diseases collectively known as leishmaniases. The primary hosts of Leishmania are sylvatic mammals of several orders (Rodentia, Marsupialia, Carnivora, etc.). Under certain circumstances, particularly in peridomestic and domestic transmission foci, synanthropic and domestic animals can act as source of infection for phlebotomine sand fly vectors. Dogs have long been implicated as the main domestic reservoirs of Leishmania (Leishmania) infantum, the aetiological agent of zoonotic visceral leishmaniasis, and there exists an increasing trend to regard dogs as the main domestic reservoirs of Leishmania (Viannia) braziliensis, the most widespread aetiological agent of American tegumentary leishmaniasis. However, insights derived from recent research indicate that not dogs but humans are probably the most important domestic reservoirs of L. (V.) braziliensis. In the present article, the role of dogs as reservoirs of Leishmania parasites, with emphasis on L. (L.) infantum and L. (V.) braziliensis, is reviewed.

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Author and article information

Contributors

Rossella Panarese: rossella.panarese@gmail.com

Roberta Iatta: roberta.iatta@uniba.it

Jairo Alfonso Mendoza-Roldan: ja.mendozaroldan@gmail.com

Andrea Zatelli: andrea.zatelli@uniba.it

Frederic Beugnet: Frederic.BEUGNET@boehringer-ingelheim.com

Domenico Otranto:

ORCID: http://orcid.org/0000-0002-7518-476X

domenico.otranto@uniba.it

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 29 July 2021

Publication date PMC-release: 29 July 2021

Publication date Collection: 2021

Volume: 14

Electronic Location Identifier: 381

Affiliations

[1 ]GRID grid.7644.1, ISNI 0000 0001 0120 3326, Department of Veterinary Medicine, , University of Bari, ; Valenzano, Italy

[2 ]GRID grid.484445.d, ISNI 0000 0004 0544 6220, Boehringer Ingelheim Animal Health, ; Lyon, France

[3 ]GRID grid.411807.b, ISNI 0000 0000 9828 9578, Faculty of Veterinary Sciences, , Bu-Ali Sina University, ; Hamedan, Iran

Author information

Domenico Otranto http://orcid.org/0000-0002-7518-476X

Article

Publisher ID: 4883

DOI: 10.1186/s13071-021-04883-3

PMC ID: 8323259

PubMed ID: 34325730

SO-VID: 2ee3b384-63fc-42c1-bbf2-d6f13a76f1f2

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 5 May 2021

Date accepted : 20 July 2021

Funding

Funded by: Boehringer Ingelheim Animal Health (FR)

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: dirofilariosis,leishmaniosis,incidence,insecticide,afoxolaner,nexgard®,chemoprophylaxis

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ScienceOpen disciplines: Parasitology

Keywords: dirofilariosis, leishmaniosis, incidence, insecticide, afoxolaner, nexgard®, chemoprophylaxis

Efficacy of afoxolaner (NexGard®) in preventing the transmission of Leishmania infantum and Dirofilaria immitis to sheltered dogs in a highly endemic area

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Malaria vaccine development

Most cited references 43

Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern.

Human and animal dirofilariasis: the emergence of a zoonotic mosaic.

The role of dogs as reservoirs of Leishmania parasites, with emphasis on Leishmania (Leishmania) infantum and Leishmania (Viannia) braziliensis.

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