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The occurrence of Dirofilaria immitis, Borrelia burgdorferi, Ehrlichia canis and Anaplasma phagocytophium in dogs in China

Published online by Cambridge University Press:  11 May 2011

Z. Xia,
D. Yu,
J. Mao,
Z. Zhang and
J. Yu
Z. Xia*
Affiliation:
Internal Medicine Laboratory, Department of Veterinary Clinical Medicine, College of Veterinary Medicine, China Agricultural University, Beijing, People's Republic of China
D. Yu
Affiliation:
Internal Medicine Laboratory, Department of Veterinary Clinical Medicine, College of Veterinary Medicine, China Agricultural University, Beijing, People's Republic of China
J. Mao
Affiliation:
Shanghai Family Pet Hospital, Shanghai, People's Republic of China
Z. Zhang
Affiliation:
Beijing Aikang Pet Hospital, Beijing, People's Republic of China
J. Yu
Affiliation:
Animal Department, Beijing Aquarium, Beijing, People's Republic of China
*
*Fax: +86 −010-62732804 E-mail: drxia@126.com
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Abstract

A survey of the occurrence of Dirofilaria immitis, Borrelia burgdorferi, Ehrlichia canis and Anaplasma phagocytophium in dogs was undertaken in the People's Republic of China between October 2008 and October 2009. A total of 600 blood samples were taken from dogs in four cities in China: 300 in Beijing, 150 in Shenzhen, 30 in Shanghai and 120 in Zhengzhou. All samples were tested for the heartworm antigen and antibodies of canine B. burgdorferi, E. canis and A. phagocytophium by using the canine SNAP® 4Dx® test kit. The occurrence of D. immitis, B. burgdorferi, E. canis and A. phagocytophium was 1.17% (7/600), 0.17% (1/600), 2.17% (13/600) and 0.5% (3/600), respectively. In Shenzhen city 2% (3/150), 8.67% (13/150) and 2% (3/150) of samples were positive for D. immitis, E. canis and A. phagocytophium, respectively. The occurrence of heartworm antigen was 0.33% (1/300) in Beijing, 2.00% (3/150) in Shenzhen, 3.33% (1/30) in Shanghai and 1.67% (2/120) in Zhengzhou. We found E. canis and A. phagocytophium only at one site, Shenzhen, while the only occurrence of B. burgdorferi was at Beijing. In conclusion, the dog population in China is at potential risk for D. immitis, B. burgdorferi, E. canis and A. phagocytophium infection, the risk being especially high in southern China.

Information

Type
Research Papers
Information
Journal of Helminthology , Volume 86 , Issue 2 , June 2012, pp. 185 - 189
Copyright
Copyright © Cambridge University Press 2011

Introduction

Canine heartworm disease, ehrlichiosis, Lyme disease and anaplasmosis are all vector-borne diseases (Beugnet & Marie, Reference Beugnet and Marie2009) transmitted mainly via ticks and mosquitoes. They occur worldwide, with geographic variation, in countries such as the USA (Beall et al., Reference Beall, Chandrashekar, Eberts, Cyr, Diniz, Mainville, Hegarty, Crawford and Breitschwerdt2008; Bowman et al., Reference Bowman, Little, Lorentzen, Shields, Sullivan and Carlin2009), France (Pantchev et al., Reference Pantchev, Schaper, Limousin, Norden, Weise and Lorentzen2009b), Germany (Gothe, Reference Gothe1998; Pantchev et al., Reference Pantchev, Norden, Lorentzen, Rossi, Rossi, Brand and Dyachenko2009a), Brazil (Trapp et al., Reference Trapp, Dagnone, Vidotto, Freire, Amude and de Morais2006; Costa et al., Reference Costa, Rembeck, Ribeiro, Beelitz, Pfister and Passos2007), Israel (Levi et al., Reference Levi, Waner, Baneth, Keysary, Bruchim, Silverman and Harrus2006), Sweden (Egenvall et al., Reference Egenvall, Bonnett, Gunnarsson, Hedhammar, Shoukri, Bornstein and Artursson2000), Spain (Montoya et al., Reference Montoya, Morales, Ferrer, Molina and Corbera1998; Amusategui et al., Reference Amusategui, Tesouro, Kakoma and Sainz2008; Tabar et al., Reference Tabar, Francino, Altet, Sanchez, Ferrer and Roura2009) and Turkey (Yildirim et al., Reference Yildirim, Ica, Atalay, Duzlu and Inci2007; Bhide et al., Reference Bhide, Yilmaz, Golcu, Torun and Mikula2008), where they can be detected in veterinary clinical practice.

Heartworm disease is caused by Dirofilaria immitis and diagnosed by the detection of circulating microfilariae in blood smears and other methods (de Caprariis et al., Reference de Caprariis, Sasanelli, Paradies, Otranto and Lia2009; Miterpakova et al., Reference Miterpakova, Antolova, Hurnikova, Dubinsky, Pavlacka and Nemeth2010). Lyme disease and anaplasmosis are caused by Borrelia burgdorferi and Anaplasma phagocytophium, both of them being transmitted by Ixodes spp. (Morshed et al., Reference Morshed, Scott, Fernando, Geddes, McNabb, Mak and Durden2006). Ehrlichiosis is caused by Ehrlichia canis, an obligate intracellular bacterium transmitted by the brown dog tick, with a tropism for haematopoietic cells (Skotarczak, Reference Skotarczak2003).

During the past three decades, there has been an increase in the number of different breeds of both pet dogs and working dogs in China. We decided to investigate the occurrence of D. immitis, B. burgdorferi, E. canis and A. phagocytophium in dogs with a study covering four Chinese cities – Beijing, the capital of China (39°57′N, 116°17′E); Shenzhen (22°33′N, 114°07′E), located in southern China; Shanghai (31°11′N, 121°29′E), located in eastern China; and Zhengzhou (34°44′N, 113°42′E), located in central China (fig. 1).

Fig. 1

Map of China showing the four cities where blood samples were collected from dogs.

Materials and methods

Collection of serum samples

Canine blood samples (n = 600) were collected from the jugular vein or lateral saphenous vein by local veterinary practitioners between October 2008 and October 2009 at animal hospitals with a significant number of pet patients: Beijing (n = 300), Shenzhen (n = 150), Shanghai (n = 30) and Zhengzhou (n = 120). There were five locations in different areas of Beijing: China Agriculture University, Beijing Companion Pet Hospital, Beijing Aikang Pet Hospital, Xiao Tong Shan Animal Shelter and Beijing Police Dog Base. In Shenzhen city, the six chosen animal hospitals were Beibei Pet Hospital, Australia Animal Hospital, Kant Animal Hospital, Interest Animal Hospital, Loyalty Pet Hospital and Qiao Cheng Aozhou Pet Hospital; 30 blood samples were tested at each hospital. Shanghai Family Pet Hospital (in Shanghai) and Zhengzhou Kangxu Animal Hospital (in Zhengzhou) also took part in the collection of blood samples. The blood samples were centrifuged at 1000 g for 10 min and serum was obtained, frozen and stored at − 20°C until analysis.

For samples collected in Beijing city, the breed, age, sex, living environment, type of use and the locations of purchase were obtained for each dog using a questionnaire provided to the local veterinarians at the time of blood collection. However, this detailed information was not collected in the other three cities. The owners agreed with publication of the data.

Of the 300 dogs in the Beijing survey, 35 different breeds were identified: Pekinese (63 cases, 21%); German shepherd (18.3%); mixed breed (10.7%); English springer spaniel (5.7%); Shih Tzu (5%); poodle (4%); chow chow (4%); Pomeranian (3.3%); golden retriever (3%); Labrador retriever (2.7%); cocker spaniel (2.7%); Tibetan mastiff (2%); schnauzer (1.7%); husky (1.7%); Yorkshire terrier (1.3%); Doberman (1%); bulldog (1%); dachshund (1%); St Bernard (1%); West Highland white terrier (0.7%); basset hound (0.7%); pug (0.7%); chihuahua (0.7%); Old English shepherd (0.7%); Welsh corgi (0.7%); Rottweiler (0.7%); Afghan hound (0.3%); mini Doberman (0.3%); Caucasian Ovcharka (0.3%); Shiba (0.3%); greyhound (0.3%); border collie (0.3%); Japanese spitz (0.3%); Shetland sheepdog (0.3%); and Scottish terrier (0.3%). A total of 185 were male (61.7%) and 115 were female (38.3%). The average age was 5 years (ranged from 8 months to 16 years). Of the 300 dogs, 25 (8.3%) were tested during spring (March–May), 99 (33%) were tested during summer (June–August), 161 (53.7%) were tested during autumn (September–November) and 15 (5%) were tested during winter (December–February). One hundred and ninety-six dogs were housed indoors (65.3%), 99 were housed outdoors (33%) and five dogs were housed both indoors and outdoors (1.7%). Three types of dogs participated in this survey: work dogs (80 dogs, 26.7%, n = 300); companion pet dogs (190 dogs, 63.3%, n = 300); and shelter dogs (30 dogs, 10%). There were 216 dogs (72%) purchased in Beijing, China, 73 dogs (24.3%) purchased from other provinces or districts and 11 dogs (3.7%) imported from other countries.

Determination of antigens and antibodies

Heartworm disease antigen, and antibodies of canine B. burgdorferi, E. canis and A. phagocytophium were determined using the canine SNAP® 4Dx® test kit (IDEXX Laboratory Inc., Westbrook, Maine, USA) according to the manufacturer's instructions. The tests were performed by the laboratory staff in the animal hospitals.

Data analysis

The data were analysed using SPSS software (version 12.0; SPSS Inc., Chicago, Illinois, USA). The results are shown as mean values and standard deviations.

Results

The occurrence of D. immitis, B. burgdorferi, E. canis and A. phagocytophium was 1.17% (7/600), 0.17% (1/600), 2.17% (13/600) and 0.50% (3/600), respectively. Among the seven dogs found with heartworm antigen, one male Labrador retriever (aged 2 years, living in Beijing) had been purchased from Hong Kong District. Also, the antibody to B. burgdorferi was detected in only one dog (0.3%), a female German shepherd (aged 3 years, living in Beijing) which had been purchased from Europe. Both of the above-mentioned dogs were tested in the autumn, lived outdoors and were working animals. The occurrence of D. immitis, E. canis and A. phagocytophium was 2.00% (3/150), 8.67% (13/150) and 2.00% (3/150), respectively, in Shenzhen city. The occurrence of heartworm antigen was 0.33% (1/300), 2.00% (3/150), 3.33% (1/30) and 1.67% (2/120) in Beijing, Shenzhen, Shanghai and Zhengzhou city, respectively. Four police dogs (13.33%, 4/30) that had antibodies to E. canis lived in a base that was located in Shenzhen. The dog living in Shanghai that tested positive to D. immitis had originated from abroad.

Discussion

Dirofilaria immitis, B. burgdorferi, E. canis and A. phagocytophium can cause vector-borne diseases, and pose significant health risks to both animals and humans. Dogs can serve as sentinels to identify the presence of vector-borne micro-organisms of both veterinary and public health significance (Bowman et al., Reference Bowman, Little, Lorentzen, Shields, Sullivan and Carlin2009). The occurrence of D. immitis, B. burgdorferi, E. canis and A. phagocytophium has been studied in many countries, with differing results. During the present study, the occurrence of D. immitis in dogs in China was 1.17%, similar to the average results (1.20%) from the IDEXX Laboratories Reference Laboratory Network (Lorentzen & Caola, Reference Lorentzen and Caola2008). However, in south Turkey, Yaman et al. (Reference Yaman, Guzel, Koltas, Demirkazik and Aktas2009) reported that the prevalence of D. immitis was 26.00%. Another study from France found that the occurrence for D. immitis was only 0.22% (Pantchev et al., Reference Pantchev, Schaper, Limousin, Norden, Weise and Lorentzen2009b). The present study has shown that heartworm antigen was found in all the four cities that we surveyed in China, implying that D. immitis infection may be widespread in China; some researchers have suggested that climatic changes and an increasing movement of pets across Europe have contributed to an increase in the geographical range of several vector-borne parasites (Genchi et al., Reference Genchi, Rinaldi, Mortarino, Genchi and Cringoli2009). Seasons and the mosquito life history could also influence the D. immitis infection (Mortarino et al., Reference Mortarino, Musella, Costa, Genchi, Cringoli and Rinaldi2008). In the present study, we found that one male Labrador retriever living in Beijing had been purchased from Hong Kong District. In addition, there were in excess of 30 days when the air temperature was more than 14°C in all the four cities surveyed, which would encourage the transmission of D. immitis (Genchi et al., Reference Genchi, Rinaldi, Mortarino, Genchi and Cringoli2009). In addition, our results show that occurrences of the disease were significantly lower than found in a previous Chinese study published in 1937 (Andrews, Reference Andrews1937). The reasons are many: improvement of dog food quality and living environments, different uses of small animals, such as companion and guard, more professional animal care and welfare; these changes may decrease the infection rate of vector-borne diseases. Further studies are required to investigate the prevalence in other regions in the future.

The occurrence of B. burgdorferi was 0.17% in the present study and was much lower than that (4.00–6.70%) of dogs from the upper Midwest and north-east of America (Bowman et al., Reference Bowman, Little, Lorentzen, Shields, Sullivan and Carlin2009), the Czech Republic (6.50%; Pejchalova et al., Reference Pejchalova, Zakovska, Fucik and Schanilec2006), Turkey (23.20%; Bhide et al., Reference Bhide, Yilmaz, Golcu, Torun and Mikula2008) and Sweden (3.90%; Egenvall et al., Reference Egenvall, Bonnett, Gunnarsson, Hedhammar, Shoukri, Bornstein and Artursson2000). The only positive test for B. burgdorferi was detected in Beijing; the dog had been purchased from Europe and was possibly a carrier of B. burgdorferi before arriving in China.

There have been many reports about the seroprevalence of E. canis. M'Ghirbi et al. (Reference M'Ghirbi, Ghorbel, Amouri, Nebaoui, Haddad and Bouattour2009) found that 54.20% of test samples were seropositive for E. canis in Tunisia, whereas 23.00% of dogs were seropositive for E. canis antibodies in southern Brazil (Trapp et al., Reference Trapp, Dagnone, Vidotto, Freire, Amude and de Morais2006). These results are not in line with those of the present study (2.17%). All dogs testing positive for E. canis were detected in Shenzhen, a city located in the subtropics. From a study by Hua et al. (Reference Hua, Yuhai, Shide, Yang, Bohai and Xiangrui2000), canine ehrlichiosis has occurred in the suburbs of Guangzhou since 1998, and the causative agents were E. canis and E. platys. As Shenzhen is located in the same region as Guangzhou, it may be an endemic area for E. canis. Wen et al. (Reference Wen, Cao and Pan2003) identified a variety of tick-borne Ehrlichia agents and proved that these diseases exist in China.

The present study detected the occurrence of A. phagocytophium (0.50%; three cases that were found in Shenzhen), which is contradicted by the results from the USA (5.50–11.60%; Bowman et al., Reference Bowman, Little, Lorentzen, Shields, Sullivan and Carlin2009) and from Italy (8.76%; Ebani et al., Reference Ebani, Cerri, Fratini, Ampola and Andreani2008).

The infections of D. immitis, B. burgdorferi, E. canis and A. phagocytophium have a worldwide geographic distribution, occurring especially in tropical and subtropical regions with an abundance of special ticks and mosquitoes that are vectors of these pathogens (Costa et al., Reference Costa, Rembeck, Ribeiro, Beelitz, Pfister and Passos2007). Shenzhen city is located in the subtropical region of southern China. Three kinds of vector-borne disease agents (D. immitis, E. canis and A. phagocytophium) were found in Shenzhen city, which might be related to the local climate or to haematophagous arthropods. Further investigation is therefore required.

In conclusion, this is the first study to investigate the occurrence of vector-borne pathogens in China. The dog populations have risks for D. immitis, B. burgdorferi, E. canis and A. phagocytophium infection in China, with the risk being especially high in southern China. The present study had its limitations: there were insufficient samples; there were incomplete records of the dogs' backgrounds that led to us not being able to compare the data; we did not know the species of vectors involved; and many specific prevalence factors related to the situation in China were not clear. Future studies need to be more extensive.

Acknowledgements

We would like to thank local veterinary practitioners for collecting blood samples and IDEXX Laboratories Inc. for freely providing the test kits.

References

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Figure 0

Fig. 1Map of China showing the four cities where blood samples were collected from dogs.