Volume 21, 2014
|Number of page(s)||3|
|Published online||03 March 2014|
Prevalence of Dirofilaria immitis among shelter dogs in Tokyo, Japan, after a decade: comparison of 1999–2001 and 2009–2011
Prévalence de Dirofilaria immitis chez les chiens en chenil à Tokyo (Japon) après une décennie : comparaison de 1999–2001 et 2009–2011
Laboratory of Medical Zoology, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa
2 Tokyo Metropolitan Institute of Public Health, 3–24–1 Hyakunincho, Shinjuku, Tokyo 169-0073, Japan
3 Merial Japan Limited, 3–20–2 Nishi Shinjyuku, Shinjyuku, Tokyo 163-1488, Japan
4 Laboratory of Infectious Diseases and Immunology, College of Veterinary Medicine, Nippon Veterinary and Life Science University, 1–7–1 Kyonancho, Musashino, Tokyo 180-8602, Japan
* Corresponding author: email@example.com
Accepted: 11 February 2014
Changes in the seroprevalence of Dirofilaria immitis infection among shelter dogs between a decade ago and the present were evaluated. Serum samples were collected from 200 adult dogs in urban and suburban areas in Tokyo, Japan, during two 2-year periods (April 1999 to March 2001 and April 2009 to March 2011). Sera were tested for the presence of D. immitis antigen using a specific commercialized kit. The seroprevalence of D. immitis infection was 46% in 1999–2001 and 23% in 2009–2011. A decrease was observed in the prevalence of infection between 1999–2001 and 2009–2011; in particular, the prevalence in urban areas decreased significantly compared with that in suburban areas (P < 0.01). There was no significant difference in prevalence between the sexes in each period, but there was a significant difference between mixed-breed and purebred dogs (P < 0.01). The decrease in prevalence of canine heartworm disease in urban areas could be related to better veterinary care.
Les changements de séroprévalence d’infection à Dirofilaria immitis parmi les chiens en chenil ont été évaluées il y a une décennie et récemment. Des sérums provenant de 200 chiens adultes ont été collectés dans des zones urbaines ou péri-urbaines de Tokyo pendant deux périodes de deux ans (Avril 1999–Mars 2001 et Avril 2009–Mars 2011). Les sérums ont été testés pour la présence d’antigènes de D. immitis. La séroprévalence de l’infection par D. immitis était de 46 % en 1999–2001 et 23 % sur la période 2009–2011. Une diminution de la prévalence a été observée entre 1999–2001 et 2009–2011. En particulier, la prévalence en zones urbaines a significativement diminué par rapport à celle des zones péri-urbaines (P < 0.01). Aucune différence significative n’a été notée entre les sexes pour chaque période mais il y avait une différence significative entre les chiens de race et les autres (P < 0.01). La diminution de prévalence de la dirofilariose canine observée en zone urbaine pourrait être liée à un meilleur suivi vétérinaire.
Key words: Canine heartworm disease / Chemoprophylaxis / Dirofilaria immitis / Dog / Epidemiology
© M. Oi et al., published by EDP Sciences, 2014
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Cardiopulmonary dirofilariosis is a parasitic disease with a worldwide distribution caused by Dirofilaria immitis Leidy, 1856 , a nematode that is transmitted by mosquitoes. The adult worms are commonly found in the pulmonary arteries and right ventricle of dogs, and result in pathological damage, such as edema, ascites, arrhythmia, tachyarrhythmia, and even death of infected dogs . The increasing temperatures caused by climate change and global warming can affect the distribution and density of mosquitoes, and consequently the transmission and spread of mosquito-borne diseases, such as dirofilariosis caused by D. immitis [3, 5]. Predictive models in Europe and Argentina have demonstrated an actual risk of spread of Dirofilaria spp. infections into areas previously free from the disease [4, 5, 11, 14].
In Japan, D. immitis infection of dogs has been considered to be prevalent since the earliest report on canine dirofilariosis in 1880 . In the latest study, Nogami and Sato  reported a prevalence rate of 46.8% in shelter dogs tested at necropsy from 1989 to 1995. However, current epidemiological information on the prevalence of D. immitis infection is limited. The present study was conducted to determine the prevalence of D. immitis infection among shelter dogs in Tokyo, Japan, in order to evaluate the modifications in the prevalence between the present and a decade ago, and between urban and suburban areas.
The present study was carried out in Tokyo, Japan (Figure 1). Canine serum samples were obtained from 200 adult shelter dogs kept in the Tokyo Metropolitan Animal Care and Consultation Center (Permission No. 22-2350). All sampling procedures were performed by shelter veterinarians in accordance with the Guidelines on research and survey using animals at Tokyo Metropolitan Animal Care and Consultation Center. This included samples from 100 dogs from April 1999 to March 2001, and 100 dogs from April 2009 to March 2011. A questionnaire including sex, estimated age, breed, and housing area (urban or suburban) was collected for each dog. Serum was stored at −30 °C until assay. All samples were tested for circulating D. immitis antigen using a specific commercialized immunochromatography kit (Solo Step® CH; Heska Co., Loveland, CO, USA) according to the manufacturer’s instructions.
Urban and suburban areas: regions of origin of the shelter dogs tested for Dirofilaria immtis infection.
The data were analyzed to evaluate the differences between proportions of dogs infected with D. immitis using the chi-square test. In all analyses, P < 0.05 was taken to indicate statistical significance.
The research area, sex and breed of distribution in dogs with D. immitis infection are shown in Table 1. The overall prevalence rates of D. immitis infection were 46.0% in 1999–2001 and 23.0% in 2009–2011 (P < 0.01). The prevalence rates of infection in urban areas were 46.0% in 1999–2001 and 18.2% in 2009–2011 (P < 0.01), and those in suburban areas were 46.0% and 28.9% (P > 0.05), respectively. There was no significant difference in prevalence between male and female dogs between the periods. The prevalence rates in mixed-breed dogs were 58.5% in 1999–2001 and 50.0% in 2009–2011, while those in purebred dogs were 22.9% and 10.3%, respectively. Significant differences (P < 0.01) in prevalence were observed between mixed-breed and purebred dogs in both periods.
Seroprevalence of Dirofilaria immitis infection in shelter dogs in April 1999 to March 2001 and April 2009 to March 2011 in Tokyo, Japan.
In the present study, a significant decrease from 46.0% to 23.0% was observed in the overall prevalence of D. immitis infection in Tokyo over the past decade. During the past decade, various types of macrocyclic lactones for D. immitis prevention have come into use worldwide, and the increased use of chemoprophylaxis is probably the major factor responsible for the decrease in prevalence of D. immitis infection in Tokyo. However, there are contrasting results in terms of breeds. The prevalence of infection in purebreds decreased by half over the past decade (22.9% in 1999–2001 and 10.3% in 2009–2011), while the infection in mixed breeds was still highly prevalent (58.5% in 1999–2001 and 50.0% in 2009–2011). This could reflect a higher rate of chemoprophylaxis in the purebred canine population than that in the mixed-breed canine population in Tokyo.
Decreases in prevalence of D. immitis infection were observed in both urban and suburban areas. These findings suggest that the prevalence of infection is markedly affected by veterinary care. The decreased prevalence, particularly in urban areas, has been conspicuous compared with that in suburban areas. This is because the rate of purebred populations in the urban areas increased and most of these dogs probably received chemoprophylaxis. Alternatively, urban areas with less parks may be more susceptible to changes in the environment than suburban areas.
The results of the present study were compared with those of other studies performed in different countries on approximately the same latitude as Japan. The prevalence of D. immitis infection in dogs in these countries varied markedly: 6.9%–20.9% in Korea [7, 13], 0.33%–3.33% in China , 3.6%–8.9% in Portugal , 34.13% in Greece , and 1%–12.5% in the United States . The present study demonstrated that D. immitis infection is endemic in Japan. The differences in prevalence among countries may be due to the differences in density of vectors, density of the parasite reservoir, and rate of prevention in dogs. This is the first study to evaluate changes in the seroprevalence of D. immitis infection in a metropolitan city over the past decade.
The authors declare that there are no conflicts of interest.
The authors thank the staff of the Tokyo Metropolitan Animal Care and Consultation Center for their help with sampling of the dogs included in this study. This work was financially supported in part by the Research and Development Program for New Bioindustry Initiatives, the National Agriculture and Food Research Organization, Japan, and the Academic Frontier Project for Private Universities from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
- Aoyama K. 1880. Parasite of the canine heart. The Iji-Shimbun, 29, 23. [Google Scholar]
- Cardoso L, Mendao C, de Carvalho LM. 2012. Prevalence of Dirofilaria immitis, Ehrlichia canis, Borrelia burgdorferi sensu lato, Anaplasma spp. and Leishmania infantum in apparently healthy and CVBD-suspect dogs in Portugal. Parasites and Vectors, 5, 62. [CrossRef] [Google Scholar]
- Genchi C, Mortarino M, Rinaldi L, Cringoli G, Traldi G, Genchi M. 2011. Changing climate and changing vector-borne disease distribution, the example of Dirofilaria in Europe. Veterinary Parasitology, 176(4), 295–299. [CrossRef] [PubMed] [Google Scholar]
- Genchi C, Rinaldi L, Cascone C, Mortarino M, Cringoli G. 2005. Is heartworm really spreading in Europe? Veterinary Parasitology, 133(2–3), 137–148. [CrossRef] [PubMed] [Google Scholar]
- Genchi C, Rinaldi L, Mortarino M, Genchi M, Cringoli G. 2009. Climate and Dirofilaria infection in Europe. Veterinary Parasitology, 163(4), 286–292. [CrossRef] [PubMed] [Google Scholar]
- Founta A, Theodoridis Y, Frydas S, Chliounakis S. 1999. The presence of filarial parasites of dogs in Serrae Province. Journal of the Hellenic Veterinary Medical Society, 50(4), 315–320. [Google Scholar]
- Jung BY, Gebeyehu EB, Seo MG, Byun JW, Kim HY, Kwak D. 2012. Prevalence of vector-borne diseases in shelter dogs in Korea. Veterinary Record, 171(10), 249. [CrossRef] [Google Scholar]
- Lee ACY, Montgomery SP, Theis JH, Blagburn BL, Eberhard ML. 2010. Public health issues concerning the widespread distribution of canine heartworm disease. Trends in Parasitology, 26(4), 168–173. [CrossRef] [PubMed] [Google Scholar]
- Leidy J. 1856. A synopsis of entozoa and some of their ecto-congeners observed by the author. Proceedings of the Academy of Natural Sciences of Philadelphia, 8, 42–58. [Google Scholar]
- McCall JW, Genchi C, Kramer LH, Guerrero J, Venco L. 2008. Heartworm disease in animals and humans. Advances in Parasitology, 66, 193–285. [CrossRef] [PubMed] [Google Scholar]
- Medlock JM, Barrass I, Kerrod E, Taylor MA, Leach S. 2007. Analysis of climatic predictions for extrinsic incubation of Dirofilaria in the United Kingdom. Vector-Borne and Zoonotic Diseases, 7(1), 4–14. [CrossRef] [Google Scholar]
- Nogami S, Sato T. 1997. Prevalence of Dirofilaria immitis infection in cats in Saitama, Japan. Journal of Veterinary Medical Science, 59(10), 869–871. [CrossRef] [Google Scholar]
- Song KH, Park JE, Lee DH, Lee SH, Shin HJ. 2010. Serological update and molecular characterization of Dirofilaria immitis in dogs, South Korea. Research in Veterinary Science, 88(3), 467–469. [CrossRef] [PubMed] [Google Scholar]
- Vezzani D, Carbajo AE. 2006. Spatial and temporal transmission risk of Dirofilaria immitis in Argentina. International Journal for Parasitology, 36(14), 1463–1472. [CrossRef] [PubMed] [Google Scholar]
- Xia Z, Yu D, Mao J, Zhang Z, Yu J. 2011. The occurrence of Dirofilaria immitis, Borrelia burgdorferi, Ehrlichia canis and Anaplasma phagocytophium in dogs in China. Journal of Helminthology, 86(2), 185–189. [CrossRef] [PubMed] [Google Scholar]
Cite this article as: Oi M, Yoshikawa S, Ichikawa Y, Nakagaki K, Matsumoto J & Nogami S: Prevalence of Dirofilaria immitis among shelter dogs in Tokyo, Japan, after a decade: comparison of 1999–2001 and 2009–2011. Parasite, 2014, 21, 10.
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