Re-evaluation of the species of hookworms infecting dogs in Central Vietnam

Particle and Fibre Toxicology

Rebecca J Traub¹  Dien Van Nguyen³  Trong Van Nguyen³  Van-Anh T Nguyen³  Sze Fui Hii²  Dinh Ng-Nguyen¹ 

[1] Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville 3052, VIC, Australia;School of Veterinary Science, The University of Queensland, Gatton 4343, Australia;Faculty of Animal Science and Veterinary Medicine, Tay Nguyen University, Buon Ma Thuot, Dak Lak, Vietnam

关键词: Ancylostoma;    Zoonosis;    Dog;    Hookworm;   

Others  :  1222135
DOI  :  10.1186/s13071-015-1015-y

 received in 2015-04-28, accepted in 2015-07-19,  发布年份 2015

【 摘 要 】

Background

Differentiation of canine hookworm species is crucial from both a veterinary and public health standpoint. In Vietnam, three hookworm species, namely Ancylostoma caninum, Ancylostoma braziliense and Uncinaria stenocephala are reported to infect dogs. In light of the emerging distribution of A. ceylanicum in Asia, this study aims to re-evaluate the status of Ancylostoma in dogs in Vietnam.

Methods

Faecal samples collected from 200 community dogs in Dak Lak province were subjected to faecal floatation for the detection of hookworm eggs. Hookworm-positive samples were subjected to a PCR-Restriction Fragment Length Polymorphism (PCR-RFLP) assay targeting the internal transcribed spacer (ITS) region of rDNA for hookworm species identification. A subset of hookworm-positive samples was also subject to haplotype characterisation at the cytochrome oxidase-1 (COX-1) gene. Detailed morphological criteria were utilised in addition to molecular markers, to identify adult hookworms recovered from necropsied dogs.

Results

Of 200 canine faecal samples, 111 (55.5 %) were positive for hookworm eggs on faecal flotation. Of these, 94/111 (84.7 %) were successfully amplified and assigned species status by PCR-RFLP targeting the ITS region. In total, 54.3 % (51/94) dogs harboured single infections with A. ceylanicum, 33.0 % (31/94) with A. caninum, and 12.7 % (12/94) harboured mixed infections with both A. ceylanicum and A. caninum. Adult worms recovered from necropsied dogs matched morphological description provided for A. ceylanicum, Looss (1911) for which the mediolateral and posteriolateral rays are parallel. Characterisation of the COX-1 gene placed all Vietnamese canine isolates of A. ceylanicum within the ‘zoonotic’ haplotype.

Conclusion

Based on this information, it is apparent that the hookworms present in dogs in Vietnam are those of A. ceylanicum and not A. braziliense. Owing to the endemic nature of this significant zoonosis in dogs, the study strongly advocates for specific identification of this hookworm in human hookworm surveys.

【 授权许可】

   
2015 Ng-Nguyen et al.

【 图 表 】

Fig. 1.

Fig. 2.

【 参考文献 】

• [1]Traub RJ. Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis. Int J Parasitol. 2013; 43(12–13):1009-1015.
• [2]Palmer CS, Traub RJ, Robertson ID, Hobbs RP, Elliot A, While L, Rees R, Thompson RC. The veterinary and public health significance of hookworm in dogs and cats in Australia and the status of A. ceylanicum. Vet Parasitol. 2007; 145(3–4):304-313.
• [3]Miller TA. Pathogenesis and immunity in hookworm infection. Trans R Soc Trop Med Hyg. 1968; 62(4):473-489.
• [4]Areekul S, Saenghirun C, Ukoskit K. Studies on the pathogenicity of Ancylostoma ceylanicum. I. Blood loss in experimental dogs. Southeast Asian J Trop Med Public Health. 1975; 6(2):235-240.
• [5]Dove WE. Further studies on Ancylostoma braziliense and the etiology of creeping eruptions. Am J Hygiene. 1932; 15:664-711.
• [6]Prociv P, Croese J. Human enteric infection with Ancylostoma caninum: hookworms reappraised in the light of a “new” zoonosis. Acta Trop. 1996; 62(1):23-44.
• [7]Hsu YC, Lin JT. Images in clinical medicine. Intestinal infestation with Ancylostoma ceylanicum. N Engl J Med. 2012; 366(13):e20.
• [8]Chung CS, Lin CK, Su KE, Liu CY, Lin CC, Liang CC, Lee TH. Diagnosis of Ancylostoma ceylanicum infestation by single-balloon enteroscopy (with video). Gastrointest Endosc. 2012; 76(3):671-672.
• [9]Inpankaew T, Schar F, Dalsgaard A, Khieu V, Chimnoi W, Chhoun C, Sok D, Marti H, Muth S, Odermatt P et al.. High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012. Emerg Infect Dis. 2014; 20(6):976-982.
• [10]Brunet J, Lemoine J, LeFebvre N, Denis J, FPfaff A, Abou-Bacar A et al. Human infection by A. ceylanicum in Myanmar. Emerg Infect Dis. 2015, accepted 21-06-2015.
• [11]Houdemer EF. Recherches de Parasitologie Comparée Indochinoise. Le Francois, Paris: 1938. p 124.
• [12]Nguyen QD. Tinh hinh nhiem giun o dan cho nuoi tai Ha Noi. [The status of roundworms infection in dogs in Ha Noi.]. Khoa Hoc Ky Thuat Thu Y [Veterinary Science and Techniques]. 2012; 19(4):25-29.
• [13]Lê H, Lương V. Giun móc ký sinh trên chó ở thành phố Hồ Chí Minh [Hookworm in dogs in Ho Chi Minh city]. Khoa Học Kỹ Thuật Thú y [Veterinary Science and Techniques]. 1998; 5(4):69-73.
• [14]Vo THL, Nguyen VT. Tình hình nhiễm giun tròn đường tiêu hóa của chó tại một số địa phương tỉnh [The status of nematode infection in dogs in Thanh Hoa province]. Khoa Hoc Ky Thuat Thu Y [Veterinary Science and Techniques]. 2011,18:66-71.
• [15]Darling S. Ancylostoma braziliense de Faria, 1910, and its occurrence in man and animals. Am J Hygiene. 1924; 4:416-448.
• [16]Biocca E. On Ancylostoma braziliense (de Faria, 1910) and its morphological differentiation from A. ceylanicum (Looss, 1911). J Helminthol. 1951; 15:1-10.
• [17]Yoshida Y, Okamoto K, Matsuo K, Kwo EH, Retnasabapathy A. The occurrence of Ancylostoma braziliense (de Faria, 1910) and Ancylostoma ceylanicum (Looss, 1911) in Malaysia. Southeast Asian J Trop Med Public Health. 1973; 4(4):498-503.
• [18]Gioi Thieu Khai Quat Ve Dak Lak [An overview about Dak Lak province]. http://chinhphu. vn/portal/page/portal/chinhphu/cactinhvathanhpho/tinhdaklak/thongtintinhthanh?view=introduction&provinceId=1355 webcite
• [19]Inpankaew T, Schar F, Khieu V, Muth S, Dalsgaard A, Marti H, Traub RJ, Odermatt P. Simple fecal flotation is a superior alternative to guadruple kato katz smear examination for the detection of hookworm eggs in human stool. PLoS Negl Trop Dis. 2014; 8(12): Article ID e3313
• [20]Yoshida Y. Comparative studies on Ancylostoma braziliense and Ancylostoma ceylanicum I. The adult stage. J Parasitol. 1971; 57(5):983-989.
• [21]Traub RJ, Robertson ID, Irwin P, Mencke N, Thompson RC. Application of a species-specific PCR-RFLP to identify Ancylostoma eggs directly from canine faeces. Vet Parasitol. 2004; 123(3–4):245-255.
• [22]Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013; 30:2725-2729.
• [23]Monnig HO. Veterinary helminthology and entomology: The diseases of domesticated animals caused by helminth andarthropod parasites. 2nd ed. Baillie’re Tindall and Cox, London, U.K.; 1938.
• [24]Lucio-Forster A, Liotta JL, Yaros JP, Briggs KR, Mohammed HO, Bowman DD. Morphological differentiation of eggs of Ancylostoma caninum, Ancylostoma tubaeforme, and Ancylostoma braziliense from dogs and cats in the United States. J Parasitol. 2012; 98(5):1041-1044.
• [25]Sheikh O, Lee C, Whitten L. A survey of helminths and arthropods in stray dogs in Kuala Lumpur. Kajian Veterinarian. 1985; 17:19-23.
• [26]Choo J, Pang E, Prociv P. Hookworms in dogs of Kuching, Sarawak (north Borneo). Trans Rl Soc TropMed Hygiene. 2000; 94(1):21-22.
• [27]Margono SS, Koesharjono C, Kosin E. Hookworm in dogs and cats in the area of Jakarta. Trop Geogr Med. 1979; 31(2):257-261.
• [28]Ngui R, Mahdy MA, Chua KH, Traub R, Lim YA. Genetic characterization of the partial mitochondrial cytochrome oxidase c subunit I (cox 1) gene of the zoonotic parasitic nematode, Ancylostoma ceylanicum from humans, dogs and cats. Acta Trop. 2013; 128(1):154-157.
• [29]Ngui R, Lim YA, Traub R, Mahmud R, Mistam MS. Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals. PLoS Negl Trop Dis. 2012; 6(2): Article ID e1522
• [30]Conlan JV, Khamlome B, Vongxay K, Elliot A, Pallant L, Sripa B, Blacksell SD, Fenwick S, Thompson RC. Soil-transmitted helminthiasis in Laos: a community-wide cross-sectional study of humans and dogs in a mass drug administration environment. Am J Trop Med Hyg. 2012; 86(4):624-634.
• [31]Traub RJ, Inpankaew T, Sutthikornchai C, Sukthana Y, Thompson RC. PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in Bangkok. Vet Parasitol. 2008; 155(1–2):67-73.