Next Article in Journal
Staphylococcus aureus-Induced Necroptosis Promotes Mitochondrial Damage in Goat Endometrial Epithelial Cells
Next Article in Special Issue
Differential Spleen miRNA Expression Profile of Beagle Dogs Infected with Toxocara canis
Previous Article in Journal
Dietary Supplemental Chromium Yeast Improved the Antioxidant Capacity, Immunity and Liver Health in Broilers under High Stocking Density
Previous Article in Special Issue
Expansion of Canine Heartworm in Spain
 
 
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Comprehensive Map of Canine Angiostrongylosis in Dogs in Spain

1
Veterinary Medicine and Therapeutic Research, Faculty of Veterinary Medicine, Research Institute of Biomedical and Health Sciences (IUIBS), University of Las Palmas de Gran Canaria, 35413 Arucas, Spain
2
Zoonotic Diseases and One Health Group, Laboratory of Parasitology, Faculty of Pharmacy, University of Salamanca, Campus Miguel Unamuno s/n, 37007 Salamanca, Spain
*
Author to whom correspondence should be addressed.
Animals 2022, 12(17), 2217; https://doi.org/10.3390/ani12172217
Received: 8 July 2022 / Revised: 15 August 2022 / Accepted: 24 August 2022 / Published: 29 August 2022
(This article belongs to the Special Issue Parasitic Diseases in Canine and Feline and Their Vectors)

Abstract

:

Simple Summary

Angiostrongylus vasorum (A. vasorum) is the causal agent of canine angiostrongylosis, an emerging disease in Europe. In Spain, A. vasorum mainly affects wild animals (red foxes and wolves), although studies in domestic dogs are scarce but show evidence of an expansion of the disease. The aim of this study was to analyze the presence of A. vasorum in domestic dogs throughout Spain, taking into account that there were still provinces where this canine infection has not been studied. Blood samples from 5544 domestic dogs were collected from January 2020 to March 2022. These samples were tested for the presence of circulating A. vasorum antigens. The overall prevalence of canine angiostrongylosis in Spain was 1.39%. No significant differences were found for sex and age, but significant differences were found for habitat. Infected domestic dogs were reported in most Spanish provinces, with lower prevalence observed for inland provinces and higher prevalence observed for provinces along the coast, where climatic factors seem to be determinant in the establishment of the parasite.

Abstract

Canine angiostrongylosis is an emerging disease caused by Angiostrongylus vasorum, mainly affecting wild carnivores and dogs. In Spain, there are studies reporting infections in foxes, wolves, and badgers in different regions of the country. However, there are hardly any publications on its prevalence in dogs. The aim of this study was to complete and update the epidemiologic map of A. vasorum in dogs in Spain. A total of 5619 canine blood samples from all autonomous cities and provinces of Spain were collected and tested for the presence of circulating A. vasorum antigens. The overall apparent prevalence of canine A. vasorum infection in Spain was 1.39%. No significant differences were found for sex or age, but significant differences between outdoor and indoor/outdoor dogs were found. A high prevalence was also observed in the northern third of the country, where an oceanic climate prevails, being humid and rainy and where abundant vegetation can be found, thus favoring the proliferation of intermediate hosts. The results suggest that A. vasorum canine infections are heterogeneously present in a large part of the territory, demonstrating its expansion throughout the country, and therefore, awareness and prevention campaigns for this disease should be promoted.

1. Introduction

Canine angiostrongylosis is a disease caused by the parasitic nematode Angiostrongylus vasorum (Baillet, 1866), which mainly affects canids, both domestic and wild, with foxes, jackals, wolves and domestic dogs being the most studied hosts [1,2]. The life cycle of the parasite is indirect, so it involves intermediate hosts, usually snails or slugs, or paratenic hosts (frogs and domestic chicken), which carry the infective larval L3 form [3,4]. The adult forms of the parasite inhabit the pulmonary arteries and the right ventricle of the heart of the definitive host, while after ingestion, the L3 migrates from the intestines to the mesenteric lymph nodes and, subsequently, after a molting period, to the right ventricle through mesenteric lymphatic vessels, the portal vein, hepatic veins, and the caudal vena cava [5,6,7]. Adult females produce eggs that embryonate and hatch within the pulmonary capillaries, where L1 penetrates the alveoli to subsequently migrate through the trachea and larynx to the oral cavity. Once there, they are swallowed, travel throughout the digestive system, and are eliminated through feces. In the environment, L1 penetrates the intermediate host and molt to the infective stage L3.
This parasite can cause a wide range of clinical signs in the infected animal, including hemorrhagic (bleeding diathesis) and neurological signs. However, the most frequent clinical presentation is cardiorespiratory by nature, caused by the presence of adults and by the migration of larvae [8,9]. Fatal infection is often associated with severe respiratory compromise, pulmonary hypertension, right heart failure, and/or hemostatic dysfunction with fatal bleeding [10]. However, some infected animals may not show clinical signs during infection, or these infection may be non-specific, making diagnosis difficult [11,12,13].
In Europe, there has been a sharp increase in the number of published cases of carnivores infected by this parasite, so canine angiostrongylosis should be considered an emerging disease [2,14]. It is likely that this increment is influenced by increases in temperature and humidity, due to climate change, which favor the development of intermediate hosts. In addition, other factors may be influencing this emergence, such as anthropogenic factors due to changes in the use and management of land and water, or the increasingly marked urban nature of the fox, a definitive host of the parasite [2,15].
In Spain, A. vasorum has been described in foxes in the northern half of the Iberian Peninsula and in Murcia, with its prevalence ranging from 1.8% to 43.2% [16,17,18,19,20]. Other studies have also shown A. vasorum infections in wolves from the north and north-west (Asturias, Galicia, and Castilla and León) with the prevalence ranging from 2.1% to 11.6% [21,22]. Badgers have also been shown to be a definitive host of this parasite throughout the Mediterranean area [23]. More recently, two studies have been carried out in dogs in various regions of the Iberian Peninsula, where the presence of A. vasorum had been found in wild carnivores. These studies were carried out in the northern third of the Iberian Peninsula, as well as some central and coastal Mediterranean regions, reporting variable prevalence ranging from 1% to 2.74% and suggesting that this disease is underestimated in dogs [7,15]. Given the emerging nature of the disease and the results obtained previously in some Spanish regions, the objective of this study was to complete and update an epidemiologic map of A. vasorum in dogs in Spain.

2. Materials and Methods

2.1. Study Area and Climate

Spain is located in the south of Western Europe and next to North Africa, with an area of 505,370 km², being the fourth largest country in continental Europe, after Russia, Ukraine, and France [24]. Spain is organized into seventeen autonomous communities—with a total of fifty provinces—and two autonomous cities. Fifteen autonomous communities are located on the Iberian Peninsula, while the other two, made up of islands, are located in the western Mediterranean Sea (Balearic Islands) and in the Atlantic Ocean close to the northwest coast of Africa (Canary Islands). The autonomous cities (Ceuta and Melilla) are located in the north coast of the African continent, next to the Mediterranean Sea and bordering Morocco.
In peninsular Spain, the topographical relief is characterized by being high, with an average altitude of 660 meters above sea level. The mountain systems of Spain are very numerous and occupy almost half of the national territory. The terrain is articulated around a large Meseta Central (central plateau) that occupies most of the center of the Iberian Peninsula. The relief is also characterized by the depression of the Guadalquivir river, located in the southwest of the peninsula, and by the Ebro river depression, in the northeast. Moreover, Spain has a network of rivers and affluents more than 100 km in length, which run through the entire peninsula [25].
According to Köppen’s Climate Classification [26], Spain has a predominantly Mediterranean climate (Cs). Figure 1 shows a map that includes the main climates present in Spain. Most of the central-southern and northeastern coasts of the Iberian Peninsula and the Balearic Islands have a predominantly hot-summer Mediterranean climate (Csa), with mild temperatures in winter, high temperatures in summer, and irregular rainfall, depending on the geographical location. In the western autonomous communities (Asturias, Cantabria, Basque Country, La Rioja, and Navarre; northern and southern Aragon; as well as central Catalonia and the north-east of Castilla and León), the oceanic climate (Cfb) predominates, characterized by abundant rainfall throughout the year—especially in winter—and cool temperatures. The climate that predominates in Galicia and the rest of Castilla and León is a warm-summer Mediterranean climate (Csb), a temperate climate with dry and cool summers. In the southeastern coastal regions, adjoining inland areas, and the center of Aragon, the predominant climate is the cold steppe climate (BSk), a dry climate characterized as such because the amount of evaporation exceeds that of precipitation, on average. The Canary Islands have a desert climate (BWh) along the southern coasts and on the flatter islands. The mountainous islands have a hot semi-arid climate (steppe) (BSh) and BSk in the northern and inland zones, and Csa and Csb climates in the center (mountain tops) of the islands.

2.2. Sample Collection and Analysis

From January 2020 to March 2022, a total of 5619 blood samples from dogs from all autonomous communities and autonomous cities of Spain were collected. Samples were collected in 62 veterinary clinics and hospitals, which voluntarily collaborated with the study. Samples were randomly collected, provided they met the inclusion criteria. This meant that samples were obtained from both apparently healthy dogs and dogs with various clinical signs and that they were representative of the canine population admitted to Spanish practices. The distribution of collected samples is described in Table 1 and Table 2. Epidemiological data such as age, sex, and habitat were recorded for each dog. To analyze the results according to age, the dogs were grouped into 5 age groups (<1 year; 1–5 years; >5–10 years; >10–15 years and >15 years). The criteria for inclusion were (a) no previous history of angiostrongylosis, (b) not receiving prophylactic treatment against A. vasorum regularly, and (c) owner consent to participate in the survey.
Blood samples were collected from the cephalic or jugular vein, placed in 3 mL serum tubes, and centrifuged. Serum samples were kept at −20 °C until tests were performed. All samples were tested for the presence of circulating antigens of A. vasorum using Angio Detect TM (IDEXX Laboratories Inc., Westbrook, ME, USA). This qualitative rapid test was carried out following the manufacturer’s instructions.
For this study, no ethical approval was required, since all blood samples were routinely collected for official diagnostic and monitoring purposes and subsequently made available to this study. All animals were handled according to the principles of animal care required by Spanish Royal Decree 53/2013, and the study was carried out in accordance with the current Spanish and European legislation on animal protection.

2.3. Statistical Analysis

Data were analyzed using GraphPad Prism 8.4 (GraphPad, San Diego, CA, USA). Descriptive analysis of the variables considered was carried out considering the proportions of the qualitative variables. Chi-square and Fisher’s exact tests were performed to compare the proportions: Fisher’s exact test was used as a post hoc analysis of the Chi-square test. Confidence interval (95% CI) values were also calculated. In all cases, the significance level was established at p < 0.05.

3. Results

The overall apparent prevalence of canine angiostrongylosis in Spain was 1.39% (CI 95%:1.11–1.73%). The autonomous communities with the highest prevalence were Murcia (4.12%), Basque Country (3.25%), Asturias (2.50%), and Cantabria (2.40%) (Table 1). The remaining autonomous communities showed prevalence <2%, while in the Balearic Islands and in the autonomous cities of Ceuta and Melilla, no dogs were found to be positive for canine angiostrongylosis. By province, the highest prevalence was found in Bizkaia (4.80%), Murcia (4.12%), Huelva (3.85%), Cádiz (3.45%), and Teruel (3.33%) (Table 2, Figure 2). In the Canary Islands, only one dog was reported to be positive for canine angiostrongylosis, which resided on the island of Tenerife.
Table 3 shows the results based on sex, age, habitat, and climate. No statistically significant differences were found between males and females (x2 = 0.1631, df = 1, p = 0.6863). The highest prevalence was found in dogs between 1 and 10 years old, although no significant differences were found between age groups (x2 = 6.237, df = 4, p = 0.1822). Regarding the habitat of the dogs analyzed, significant differences were observed between the different groups (x2 = 8.564, df = 2, p = 0.0138), with statistically significant differences between indoor/outdoor and outdoor dogs (p = 0.0038) but not between indoor and indoor/outdoor dogs (p = 0.7693) or between indoor and outdoor dogs (p = 0.2355). When the results were analyzed according to the climate, significant differences were observed between the different groups (x2 = 11.12, df = 5, p = 0.0490), with statistically significant differences between Csa and BSh (p = 0.0257), between Csb and BSh (p = 0.0306), between Cfb and BSh (p = 0.0029), and between BSk and BSh (p = 0.0183). The highest prevalence was observed in the Cfb climate.

4. Discussion

This study provides a complete epidemiological map of canine angiostrongylosis in Spain, showing the presence of this parasite in a large part of the national territory. There have been several studies carried out in European countries that demonstrated its wide presence in countries such as Austria, Germany, Italy, Slovakia, Switzerland, Hungary, and the United Kingdom, with the prevalence ranging from 0.15% to 1.76%. In these studies, diagnoses were made based on serum antigen detection, and a prevalence similar to those in this study was reported [27,28,29,30,31,32,33], demonstrating that although prevalence is generally low, this disease is widely distributed throughout much of the continent, showing its emerging nature. Despite this, to date, there have only been two previous studies in Spain that have evaluated the presence of this disease in different regions, so an epidemiological map was needed to help determine the current status of canine angiostrongylosis in Spain [7,8,9,10,11,12,13,14,15].
When comparing the current results with reports of canine angiostrongylosis in regions that had already been studied previously, it is observed that the prevalence has remained at similar values, probably because these are relatively recent studies with similar inclusion criteria [7,15]. Previously, epidemiological data in wild carnivores have been published, demonstrating the presence of A. vasorum in regions where canine angiostrongylosis has been reported. This is the case for the autonomous communities with a Cfb climate, where previous studies have shown a high presence of this parasite in wolves and foxes [16,21]. The high rainfall that occurs in the north of the country and the extensive presence of vegetation favor the development of intermediate hosts and the infection of wild carnivores [21], which in turn act as definitive hosts favoring the infection of dogs that live in the areas, especially in rural areas.
In regions with a Bsk climate, a high prevalence has also been obtained, especially in Murcia. In these areas, the climate is semi-arid, with little annual rainfall. However, in these regions, there are large irrigated areas, such as the Ebro Valley and Murcia, with various crop protection techniques such as greenhouses, macro-tunnels (large structures made of arches of PVC pipes, usually covered with one or more layers of greenhouse plastic, agrotextile, or insect-proof netting) or micro-tunnels (plastic or spun-bonded fabric sheets placed on metal hoops over developing crops), which create the necessary conditions for the life cycle of gastropod molluscs to develop.
In general, the prevalence obtained in provinces with a Csa climate varied between 1% and 2%, being higher in some provinces, such as Huelva or Cádiz, and lower in other provinces (Madrid), whereas antigen positivity was not found in three provinces only (i.e., Girona and Balearic Islands). Given that only the predominant climates of each province have been considered, ignoring the variability of climates, and the hydrographic and orographic conditions present in each one, it is understandable that there was some variability in the results. For example, Huelva (prevalence 3.85%) and Cádiz (3.45%) have strong hydrographic components, with rivers, natural or artificial stagnant waters, marshes, and national natural parks, which, together with high temperatures, favor the development of the intermediate host.
In the Canary Islands, a case of angiostrongylosis was reported for the first time. Although this region was traditionally considered to be free of this disease, a recent study has shown the presence of the third-stage larvae of A. vasorum in different gastropods, such as Plutonia lamarckii and Cornu aspersum, in Tenerife and El Hierro [34].
The diagnostic method used has been shown to have a sensitivity of 98.1% and a specificity of 99.4% [35,36,37], which allows us to carry out a complete, precise, and exhaustive survey of the distribution of A. vasorum in Spain, thanks to excellent positive and negative predictive values (96.35% and 99.69%, respectively). The results of this study have been analyzed based on the calculation of the apparent prevalence, which has allowed us to compare and discuss the values obtained from previous studies carried out both in Spain and in other European countries [7,15,27,28,29,30,31,32,33]. However, with this diagnostic method, it is possible that some infected dogs go unnoticed, since studies have shown that experimental infections can display a negative result sooner than 9 weeks post-infection [36]. For this reason, in the case of a clinical suspicion, it is recommended to carry out diagnostic methods considered to be the gold standard, such as the Baermann test and the FLOTAC technique [38].
The results according to age indicate that the highest prevalence was found in dogs between 1 and 10 years of age. Younger dogs (less than 18 months) are generally considered to be at a higher risk of infection [33]. However, the prevalence shown by dogs less than 12 months of age in this study is lower, although in order to analyze these results, the limitations of the diagnostic test used must be taken into account, as mentioned above.
In general, there are few provinces in Spain that have obtained an apparent prevalence of 0%, which indicates how widely distributed this parasite is in the country. Canine angiostrongylosis presents a very varied clinical picture, which can make a clinical suspicion tricky for practitioners not aware of the disease. Both its respiratory and neurological clinical presentation or its presentation as a hemorrhagic diathesis can be easily confused with other more frequent or better-known pathologies. For this reason, it is necessary to create awareness and knowledge of the presence of this parasite among Spanish veterinarians, with epidemiological studies and follow-ups that show the distribution and dynamics of A. vasorum. In addition, veterinarians should include this pathology in the differential diagnosis of dogs that present compatible signs, and prevention campaigns should be promoted for animals that are at risk of infection.

5. Conclusions

This study presents a completed distribution map of A. vasorum in Spain in dogs. The parasite is heterogeneously present in a large part of the territory, demonstrating its expansion throughout the country. Bearing in mind that it is a fairly unknown disease among clinical veterinarians and among dog owners, it is quite understandable that the prevention of this pathology is not being carried out correctly in most animals, especially in those that are at higher risk. For this reason, it is necessary to carry out campaigns that stimulate preventive actions to avoid infections. Moreover, the realization of a risk map would be extremely useful, taking the bioclimatic variables provided in this study into account. For this, it would be necessary to analyze other variables (bioclimatic, vegetation, surface and underground water masses, habitats of intermediate hosts, land uses, biogeographic regions, etc.), which would expand the information provided in this study. In addition, considering that it is an emerging disease that is spreading throughout Europe, more studies are needed to address the distribution of A. vasorum in Spain, both in wild carnivores and in dogs, in order to understand the dynamics of its evolution.

Author Contributions

Conceptualization, E.C., R.M. and J.A.M.-A.; resources, E.C., R.M. and J.A.M.-A.; methodology, E.C., R.M., S.N.G.-R., J.I.M., N.C.-R. and I.R.-E.; funding acquisition, E.C., R.M. and J.A.M.-A.; writing and review, S.N.G.-R., I.R.-E., R.M. and E.C. All authors have read and agreed to the published version of the manuscript.

Funding

This study was partially supported by ELANCO SPAIN S.L (CN-240/030/159) and was funded by the Servicio Medicina Veterinaria FULP/ULPGC SD-240/030/0026. N.C.R. was supported by the “Grants for the predoctoral training program for researchers” program of the Government of the Canary Islands (TESIS2021010010), and J.I.M. was supported by the “Grants for the financing of predoctoral contracts” program of the Universidad de Las Palmas de Gran Canaria (PIFULPGC-2017-CCSALUD-3).

Institutional Review Board Statement

Ethical review and approval were not required for the animals in this study since all blood samples were routinely collected for official diagnostic and monitoring purposes and subsequently made available to this study. All animals were handled according to the principles of animal care published by Spanish Royal Decree 53/2013, and the study was carried out in accordance with the current Spanish and European legislation on animal protection.

Informed Consent Statement

Written informed consent was obtained from the owners for the participation of their animals in this study.

Data Availability Statement

The data presented in this study are available from the corresponding author upon request.

Acknowledgments

The authors thank all veterinarians who kindly collaborated and provided samples for this research. Without their collaboration and dedication, this study could not have been carried out.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

  1. Tieri, E.E.; Saletti, M.A.; D’Angelo, A.R.; Parisciani, G.; Pelini, S.; Cocco, A.; Di Teodoro, G.; Di Censo, E.; D’Alterio, N.; Latrofa, M.S.; et al. Angiostrongylus vasorum in foxes (Vulpes vulpes) and wolves (Canis lupus italicus) from Abruzzo region, Italy. Int. J. Parasitol. Parasites Wildl. 2021, 15, 184–194. [Google Scholar] [CrossRef] [PubMed]
  2. Morgan, E.R.; Modry, D.; Paredes-Esquivel, C.; Foronda, P.; Traversa, D. Angiostrongylosis in Animals and Humans in Europe. Pathogens 2021, 10, 1236. [Google Scholar] [CrossRef] [PubMed]
  3. Morgan, E.R.; Shaw, S.E.; Brennan, S.F.; De Waal, T.D.; Jones, B.R.; Mulcahy, G. Angiostrongylus vasorum: A real heartbreaker. Trends Parasitol. 2005, 21, 49–51. [Google Scholar] [CrossRef] [PubMed]
  4. Mozzer, L.R.; Lima, W.S. Gallus gallus domesticus: Paratenic host of Angiostrongylus vasorum. Vet. Parasitol. 2015, 207, 81–84. [Google Scholar] [CrossRef]
  5. Helm, J.R.; Morgan, E.R.; Jackson, M.W.; Wotton, P.; Bell, R. Canine angiostrongylosis: An emerging disease in Europe. J. Vet. Emerg. Crit. Care. (San Antonio) 2010, 20, 98–109. [Google Scholar] [CrossRef]
  6. Morgan, E.R.; Jefferies, R.; van Otterdijk, L.; McEniry, R.B.; Allen, F.; Bakewell, M.; Shaw, S.E. Angiostrongylus vasorum infection in dogs: Presentation and risk factors. Vet. Parasitol. 2010, 173, 255–261. [Google Scholar] [CrossRef]
  7. Morchón, R.; Montoya-Alonso, J.A.; Sánchez-Agudo, J.Á.; de Vicente-Bengochea, J.; Murcia-Martínez, X.; Carretón, E. Angiostrongylus vasorum in Domestic Dogs in Castilla y León, Iberian Peninsula, Spain. Animals 2021, 11, 1513. [Google Scholar] [CrossRef]
  8. Chapman, P.S.; Boag, A.K.; Guitian, J.; Boswood, A. Angiostrongylus vasorum infection in 23 dogs (1999–2002). J. Small Anim. Pract. 2004, 45, 435–440. [Google Scholar] [CrossRef]
  9. Colombo, M.; Traversa, D.; Grillotti, E.; Pezzuto, C.; De Tommaso, C.; Pampurini, F.; Schaper, R.; Drake, J.; Crisi, P.E.; Russi, I.; et al. Highly Variable Clinical Pictures in Dogs Naturally Infected with Angiostrongylus vasorum. Pathogens 2021, 10, 1372. [Google Scholar] [CrossRef]
  10. Willesen, J.L.; Langhorn, R.; Nielsen, L.N. Hemostatic Dysfunction in Dogs Naturally Infected with Angiostrongylus vasorum—A Narrative Review. Pathogens 2022, 11, 249. [Google Scholar] [CrossRef]
  11. Beugnet, F.; Halos, L.; Guillot, J. Textbook of Clinical Parasitology in Dogs and Cats; Boehringer Ingelheim: Ingelheim, Germany, 2018; p. 423. [Google Scholar]
  12. Bagardi, M.; Rabbogliatti, V.; Bassi, J.; Gioeni, D.; Oltolina, M.; Villa, L. Angiostrongylus vasorum in a Red Panda (Ailurus fulgens): Clinical Diagnostic Trial and Treatment Protocol. Acta Parasitológica 2021, 66, 282–286. [Google Scholar] [CrossRef] [PubMed]
  13. Paradies, P.; Sasanelli, M.; Capogna, A.; Mercadante, A.; Rubino, G.T.R.; Bussadori, C.M. Is Pulmonary Hypertension a Rare Condition Associated to Angiostrongylosis in Naturally Infected Dogs? Top. Companion Anim. Med. 2021, 43, 100513. [Google Scholar] [CrossRef] [PubMed]
  14. Fuehrer, H.P.; Morelli, S.; Unterköfler, M.S.; Bajer, A.; Bakran-Lebl, K.; Dwużnik-Szarek, D.; Farkas, R.; Grandi, G.; Heddergott, M.; Jokelainen, P.; et al. Dirofilaria spp. And Angiostrongylus vasorum: Current Risk of Spreading in Central and Northern Europe. Pathogens 2021, 10, 1268. [Google Scholar] [CrossRef]
  15. Carretón, E.; Morchón, R.; Falcón-Cordón, Y.; Matos, J.; Costa-Rodríguez, N.; Montoya-Alonso, J.A. First epidemiological survey of Angiostrongylus vasorum in domestic dogs from Spain. Parasit. Vectors. 2020, 13, 306. [Google Scholar] [CrossRef]
  16. Álvarez, F.; Iglesias, R.; Bos, J.; Rey, J.; San Martín Durán, M.L. Lung and hearth nematodes in some Spanish mammals. Wiad. Parazytol. 1991, 37, 481–490. [Google Scholar]
  17. Gotázar, C.; Villafuerte, R.; Lucientes, J.; Fernández-de-Luco, D. Habitat related differences in helminth parasites of red foxes in the Ebro valley. Vet. Parasitol. 1998, 80, 75–81. [Google Scholar] [CrossRef]
  18. Gerrikagoitia, X.; Barral, M.; Juste, R.A. Angiostrongylus species in wild carnivores in the Iberian Peninsula. Vet. Parasitol. 2010, 174, 175–180. [Google Scholar] [CrossRef]
  19. Mañas, S.; Ferrer, D.; Castellà, J.; Maria López-Martín, J. Cardiopulmonary helminth parasites of red foxes (Vulpes vulpes) in Catalonia, northeastern Spain. Vet. J. 2005, 169, 118–120. [Google Scholar] [CrossRef]
  20. Martínez-Carrasco, C.; Ruiz De Ybáñez, M.R.; Sagarminaga, J.L.; Garijo, M.M.; Moreno, F.; Acosta, I.; Hernández, S.; Alonso, F.D. Parasites of the red fox (Vulpes vulpes Linnaeus, 1758) in Murcia, southeast Spain. Revue Méd. Vét. 2007, 158, 331–335. [Google Scholar]
  21. Martínez-Rondán, F.J.; Ruiz de Ybáñez, M.R.; López-Beceiro, A.M.; Fidalgo, L.E.; Berriatua, E.; Lahat, L.; Sacristán, I.; Oleaga, Á.; Martínez-Carrasco, C. Cardiopulmonary nematode infections in wild canids: Does the key lie on host-prey-parasite evolution? Res. Vet. Sci. 2019, 126, 51–58. [Google Scholar] [CrossRef]
  22. Segovia, J.M.; Torres, J.; Miquel, J.; Llaneza, L.; Feliu, C. Helminths in the wolf, Canis lupus, from north-western Spain. J. Helminthol. 2001, 75, 183–192. [Google Scholar] [PubMed]
  23. Torres, J.; Miquel, J.; Motjé, M. Helminth parasites of the eurasian badger (Meles meles L.) in Spain: A biogeographic approach. Parasitol. Res. 2001, 87, 259–263. [Google Scholar] [CrossRef] [PubMed]
  24. Instituto Nacional de Estadística. Gobierno de España (INE). Available online: https://www.ine.es (accessed on 4 July 2022).
  25. Ministerio de Agricultura, Ganadería, Pesca y Alimentación. Available online: https://www.mapa.gob.es/es/default.aspx (accessed on 15 February 2022).
  26. Köppen’s Climate Classification. Available online: http://koeppen-geiger.vu-wien.ac.at/shifts.htm (accessed on 2 July 2022).
  27. Guardone, L.; Schnyder, M.; Macchioni, F.; Deplazes, P.; Magi, M. Serological detection of circulating Angiostrongylus vasorum antigen and specific antibodies in dogs from central and northern Italy. Vet. Parasitol. 2013, 192, 192–198. [Google Scholar] [CrossRef] [PubMed]
  28. Lurati, L.; Deplazes, P.; Hegglin, D.; Schnyder, M. Seroepidemiological survey and spatial analysis of the occurrence of Angiostrongylus vasorum in Swiss dogs in relation to biogeographic aspects. Vet. Parasitol. 2015, 212, 219–226. [Google Scholar] [CrossRef] [PubMed]
  29. Schnyder, M.; Schaper, R.; Pantchev, N.; Kowalska, D.; Szwedko, A.; Deplazes, P. Serological detection of circulating Angiostrongylus vasorum antigen- and parasite-specific antibodies in dogs from Poland. Parasitol. Res. 2013, 112 (Suppl. 1), 109–117. [Google Scholar] [CrossRef] [PubMed]
  30. Miterpáková, M.; Hurníková, Z.; Zalewski, A.P. The first clinically manifested case of angiostrongylosis in a dog in Slovakia. Acta Parasitol. 2014, 59, 661–665. [Google Scholar] [CrossRef] [PubMed]
  31. Deak, G.; Gillis-Germitsch, N.; Ionică, A.M.; Mara, A.; Păstrav, I.R.; Cazan, C.D.; Ioniță, M.; Mitrea, I.L.; Răileanu, C.; Bărburaș, D.; et al. The first seroepidemiological survey for Angiostrongylus vasorum in domestic dogs from Romania. Parasit. Vectors. 2019, 12, 224. [Google Scholar] [CrossRef]
  32. Globokar, M.; Pantchev, N.; Hinney, B.; Leschnik, M.; Peschke, R.; Schaper, R.; Schnyder, M. Serological and faecal detection of Angiostrongylus vasorum in dogs from Austria. Vet. Parasitol. Reg. Stud. Reports. 2021, 26, 100641. [Google Scholar] [CrossRef]
  33. Schnyder, M.; Schaper, R.; Lukácsc, Z.; Hornok, S.; Farkas, R. Combined serological detection of circulating Angiostrongylus vasorum antigen and parasite-specific antibodies in dogs from Hungary. Parasitol. Res. 2015, 114, S145–S154. [Google Scholar] [CrossRef]
  34. Segeritz, L.; Cardona, A.; Taubert, A.; Hermosilla, C.; Ruiz, A. Autochthonous Angiostrongylus cantonensis, Angiostrongylus vasorum and Aelurostrongylus abstrusus infections in native terrestrial gastropods from the Macaronesian Archipelago of Spain. Parasitol. Res. 2021, 120, 2671–2680. [Google Scholar] [CrossRef]
  35. Liu, J.; Schnyder, M.; Willesen, J.L.; Potter, A. Chandrashekar, R. Performance of the Angio Detect™ in-clinic test kit for detection of Angiostrongylus vasorum infection in dog samples from Europe. Vet. Parasitol. Reg. Stud. Rep. 2017, 7, 45–47. [Google Scholar]
  36. Schnyder, M.; Stebler, K.; Naucke, T.J.; Lorentz, S.; Deplazes, P. Evaluation of a rapid device for serological in-clinic diagnosis of canine angiostrongylosis. Parasit. Vectors 2014, 7, 72. [Google Scholar] [CrossRef] [PubMed]
  37. Venco, L.; Colaneri, G.; Formaggini, L.; De Franco, M.; Rishniw, M. Utility of thoracic ultrasonography in a rapid diagnosis of angiostrongylosis in young dogs presenting with respiratory distress. Vet. J. 2021, 271, 105649. [Google Scholar] [CrossRef] [PubMed]
  38. Cringoli, G.; Rinaldi, L.; Maurelli, M.P.; Utzinger, J. FLOTAC: New multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat. Protoc. 2010, 5, 503–515. [Google Scholar] [CrossRef]
Figure 1. Map with the main climates present in Spain (Köppen Climate Classification System). The numbers correspond to the autonomous communities and autonomous cities, as described in Table 1. Abbreviations: BSh: hot semi-arid climate (steppe); BSk: cold steppe climate; BWh: desert climate; BWk: Cold desert climate; Cfa: humid subtropical climate; Cfb: oceanic climate; Csa: hot-summer Mediterranean climate; Csb: warm-summer Mediterranean climate; Dfb: humid continental climate; Dfc: subarctic climate; Dsb: humid continental climate; Dsc: subarctic climate.
Figure 1. Map with the main climates present in Spain (Köppen Climate Classification System). The numbers correspond to the autonomous communities and autonomous cities, as described in Table 1. Abbreviations: BSh: hot semi-arid climate (steppe); BSk: cold steppe climate; BWh: desert climate; BWk: Cold desert climate; Cfa: humid subtropical climate; Cfb: oceanic climate; Csa: hot-summer Mediterranean climate; Csb: warm-summer Mediterranean climate; Dfb: humid continental climate; Dfc: subarctic climate; Dsb: humid continental climate; Dsc: subarctic climate.
Animals 12 02217 g001
Figure 2. Prevalence map for A. vasorum in domestic dogs in Spain by province and the autonomous cities of Ceuta and Melilla.
Figure 2. Prevalence map for A. vasorum in domestic dogs in Spain by province and the autonomous cities of Ceuta and Melilla.
Animals 12 02217 g002
Table 1. Prevalence of A. vasorum in dogs in Spain by autonomous communities and autonomous cities (Ceuta and Melilla). Abbreviations: n, number of dogs sampled; +, number of positive dogs; %, percentage of positive dogs (confidence interval 95%).
Table 1. Prevalence of A. vasorum in dogs in Spain by autonomous communities and autonomous cities (Ceuta and Melilla). Abbreviations: n, number of dogs sampled; +, number of positive dogs; %, percentage of positive dogs (confidence interval 95%).
n+% (CI 95%)
 1. Galicia42881.87 (0.95–3.64)
 2. Asturias12032.50 (0.85–7.09)
 3. Cantabria12532.40 (0.82–6.82)
 4. Basque Country308103.25 (1.77–5.87)
 5. Navarre17031.76 (0.60–5.06)
 6. La Rioja10011.00 (0.18–5.45)
 7. Aragón20931.44 (0.49–4.13)
 8. Catalonia52161.15 (0.53–2.49)
 9. Valencian Community35251.42 (0.61–3.28)
 10. Murcia9744.12 (1.62–10.13)
 11. Andalusia502101.99 (1.09–3.63)
 12. Castilla-La Mancha30441.32 (0.51–3.33)
 13. Extremadura15331.96 (0.67–5.61)
 14. Madrid38930.77 (0.26–2.24)
 15. Castilla and León985111.12 (0.62–1.99)
 16. Canary Islands55210.18 (0.03–1.02)
 17. Balearic Islands22900.00 (0.00–1.65)
 18. Ceuta2700.00 (0.00–12.45)
 19. Melilla4800.00 (0.00–7.41)
 Total5619781.39 (1.11–1,73)
Table 2. Prevalence of A. vasorum in dogs in Spain by province and autonomous cities (Ceuta and Melilla). Abbreviations: n, number of dogs sampled; +, number of positive dogs; %, percentage of positive dogs (confidence interval 95%).
Table 2. Prevalence of A. vasorum in dogs in Spain by province and autonomous cities (Ceuta and Melilla). Abbreviations: n, number of dogs sampled; +, number of positive dogs; %, percentage of positive dogs (confidence interval 95%).
Autonomous Community
Province
n+% (CI 95%)Autonomous Community
Province
n+% (CI 95%)
Galicia Extremadura
A Coruña22452.23 (0.96–5.12)Cáceres7111.41 (0.25–7.56)
Lugo9833.06 (1.05–8.62)Badajoz8222.44 (0.67–8.46)
Ourense4700.00 (0.00–7.56)Andalusia
Pontevedra5900.00 (0.00–6.11)Cádiz5823.45 (0.95–11.73)
Asturias Seville7011.43 (0.25–7.66)
Oviedo12032.50 (0.85–7.09)Málaga5411.85 (0.33–9.77)
Cantabria Granada8711.15 (0.20–6.23)
Santander12532.40 (0.82–6.82)Jaén6711.49 (0.26–7.98)
Basque Country Huelva7833.85 (1.32–10.71)
Araba8111.23 (0.22–6.67)Almería4100.00 (0.00–8.57)
Bizkaia12564.80 (2.22–10.08)Córdoba4712.13 (0.38–11.11)
Gipuzkoa10232.94 (1.01–8.29)Castilla-La Mancha
Navarre Albacete4000.00 (0.00–8.76)
Navarre17031.76 (0.60–5.06)Guadalajara8711.15 (0.20–6.23)
La Rioja Cuenca3800.00 (0.00–9.18)
La Rioja10011.00 (0.18–5.45)Ciudad Real8522.35 (0.65–8.18)
Aragón Toledo5411.85 (0.33–9.77)
Huesca11210.89 (0.16–4.88)Castilla y León
Zaragoza6711.49 (0.26–7.98)León14832.03 (0.69–5.79)
Teruel3013.33 (0.59–16.67)Zamora9411.06 (0.19–5.78)
Catalonia Salamanca13721.46 (0.40–5.17)
Girona7500.00 (0.00–4.87)Valladolid8500.00 (0.00–4.32)
Barcelona28531.05 (0.36–3.05)Palencia11221.79 (0.49–6.28)
Tarragona9122.20 (0.60–7.66)Burgos15431.95 (0.66–5.57)
Lleida7011.43 (0.25–7.66)Segovia9800.00 (0.00–3.77)
Valencian Community Soria8200.00 (0.00–4.47)
Castellón6011.67 (0.29–8.85)Ávila7500.00 (0.00–4.87)
Valencia20731.45 (0.49–4.17)Canary Islands
Alicante8511.18 (0.21–6.37)Las Palmas24000.00 (0.00–1.58)
Murcia S/C Tenerife31210.32 (0.06–1.79)
Murcia9744.12 (1.62–10.13)Balearic Islands
Madrid Balearic Islands22900.00 (0.00–1.65)
Madrid38930.77 (0.26–2.24)Ceuta2700.00 (0.00–12.45)
Melilla4800.00 (0.00–7.41)
Total5619781.39
Table 3. Prevalence of A. vasorum in dogs in Spain by sex, age, habitat, and climate. Abbreviations: n, number of dogs sampled; +, number of positive dogs; %, percentage of positive dogs (confidence interval 95%); BSh: hot semi-arid climate (steppe); BSk: cold steppe climate; BWh: desert climate; BWk: Cold desert climate; Cfb: oceanic climate; Csa: hot-summer Mediterranean climate; Csb: warm-summer Mediterranean climate.
Table 3. Prevalence of A. vasorum in dogs in Spain by sex, age, habitat, and climate. Abbreviations: n, number of dogs sampled; +, number of positive dogs; %, percentage of positive dogs (confidence interval 95%); BSh: hot semi-arid climate (steppe); BSk: cold steppe climate; BWh: desert climate; BWk: Cold desert climate; Cfb: oceanic climate; Csa: hot-summer Mediterranean climate; Csb: warm-summer Mediterranean climate.
n+% (CI 95%)
Sex
Female2826411.45 (1.07–1.96)
Male2793371.32 (0.96–1.82)
Age
<1 year91570.77 (0.37–1.57)
1–4.9 years1183211.78 (1.16–2.70)
5–9.9 years1389241.73 (1.16–2.56)
10–15 years1206171.41 (0.88–2.25)
>15 years92690.97 (0.51–1.84)
Habitat
Outdoor3327591.77 (1.38–2.28)
Indoor43140.93 (0.36–2.36)
Indoor/Outdoor1861150.81 (0.49–1.33)
Climates
Csa2242291.29 (0.90–1.85)
Csb1197161.34 (0.82–2.26)
Cfb1271262.05 (1.40–2.98)
BSk41771.68 (0.82–3.42)
BWh14300.00 (0.00–2.62)
BSh34900.00 (0.00–1.09)
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Carretón, E.; Morchón, R.; García-Rodríguez, S.N.; Rodríguez-Escolar, I.; Matos, J.I.; Costa-Rodríguez, N.; Montoya-Alonso, J.A. Comprehensive Map of Canine Angiostrongylosis in Dogs in Spain. Animals 2022, 12, 2217. https://doi.org/10.3390/ani12172217

AMA Style

Carretón E, Morchón R, García-Rodríguez SN, Rodríguez-Escolar I, Matos JI, Costa-Rodríguez N, Montoya-Alonso JA. Comprehensive Map of Canine Angiostrongylosis in Dogs in Spain. Animals. 2022; 12(17):2217. https://doi.org/10.3390/ani12172217

Chicago/Turabian Style

Carretón, Elena, Rodrigo Morchón, Sara Nieves García-Rodríguez, Iván Rodríguez-Escolar, Jorge Isidoro Matos, Noelia Costa-Rodríguez, and José Alberto Montoya-Alonso. 2022. "Comprehensive Map of Canine Angiostrongylosis in Dogs in Spain" Animals 12, no. 17: 2217. https://doi.org/10.3390/ani12172217

Note that from the first issue of 2016, MDPI journals use article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop