Ancylostoma ceylanicum Zoonotic Hookworm: Neglected Tropical Disease
DOI:
https://doi.org/10.14456/dcj.2021.38Keywords:
Zoonosis, Ancylostoma ceylanicum, HookwormAbstract
Hookworm infection is a parasitic disease which is important in developing countries. Most infected individuals are asymptomatic. Heavy and chronic infection cause blood loss, iron-deficiency anemia and hypoproteinemia. The disease has received little attention from public health authorities hence the term Neglected tropical diseases (NTDs). Main helminth parasites which are common infectious agent are Ancylostoma duodenale and Necator americanus. In the present, the various reports show that the disease has a secondary helminth parasite, Ancylostoma ceylanicum. A. ceylanicum is a hookworm found primarily in dogs and cats, which is common health problem in companion animals, also represents a neglected public health concern due to the incidence of the disease in humans is believed to be low. Although dogs and cats are natural host of A. ceylanicum, adult works can adapt to growing up and shedding egg in human intestines. Clinical manifestation of this infection in human also mimics that of human hookworm. Australia is interested in the pathogenesis of A. ceylanicum in humans as an emerging and re-emerging disease with increasing reports of human infections, particularly among travelers returning from travel in Southeast Asia such as Thailand, Laos, Malaysia and Myanmar which have been diagnosed by adult morphology by gastroendoscopy. Fecal examination of helminth eggs could not distinguish between A. ceylanicum, N. americanus, and A. duodenale. Epidemiological surveys of hookworm disease in this region by molecular biology indicate that Human infection with the parasite A. ceylanicum is second only to N. americanus and found that the rate of environmental contamination of A. ceylanicum was the highest among the hookworm group. Currently, the prevention of hookworm disease in humans focuses on students who are at risk groups according to the principle of eating hot food, serving spoons, washing hands, and not walking barefoot by overlooking the current incidence of A. ceylanicum infection in humans. Therefore, recognizing the importance of A. ceylanicum infection in humans from companion animals and considering the integrated control and prevention of hookworm disease with the implementation of One Health policy including people, animals and the environment will be a way to prevent the transmission of A. ceylanicum to humans and spread wider areas This can reduce the rate of hookworm infection in humans. dogs and cats in the endemic region.
References
WHO. Soil-transmitted helminth infections [Internet]. 2020 [cited 2020 Oct 16] Available from: https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections
Shepherd C, Wangchuk P, Loukas A. Of dogs and hookworms: man’s best friend and his parasites as a model for translational biomedical research. Parasites & Vectors. 2018;11:59-74.
Giudice PD, Hakimi S, Vandenbos F, Magana C, Hubiche T. Autochthonous Cutaneous Larva Migrans in France and Europe. Acta Derm Venereol. 2019;99:805–8.
Traub RJ. Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis. International Journal for Parasitology. 2013;43:1009-15.
Adugna S, Kebede T, Mekonnen Z, Degarege A, Liang S, Erko B. Diagnostic Performance of Mini Parasep® Solvent-Free Faecal Parasite Concentrator Relative to Kato-Katz and McMaster for the Diagnosis of Intestinal Parasitic Infections. Trans R Soc Trop Med Hyg. 2017;111(12):572-8.
Friedmann E, Krause-Parello CA. Companion animals and human health: benefits, challenges, and the road ahead for human–animal interaction. Rev Sci Tech Off Int Epiz. 2018;37(1):71-82.
Sato R, Fujiwara T, Kino S, Nawa N, Kawachi I. Pet Ownership and Children’s Emotional Expression: Propensity Score-Matched Analysis of Longitudinal Data from Japan. Int. J. Environ. Res. Public Health. 2019;16:758-69.
Baneth G, Thamsborg SM, Otranto D, Guillot J, Blaga R, Deplazes P, Solano-Gallego L. Major parasitic zoonoses associated with dogs and cats in Europe. Journal of Comparative Pathology. 2016;155(1): S54-S74.
Silver ZA, Kaliappan SP, Samuel P, Venugopal S, Kang G, Sarkar R, Ajjampur SSR. Geographical distribution of soil transmitted helminths and the effects of community type in South Asia and South East Asia – a systematic review. PLoS Negl Trop Dis. 2018;12(1): e0006153.
Bartsch SM, Hotez PJ, Asti L, Zapf KM, Bottazzi ME, Diemert DJ, Lee BY. The global economic and health burden of human hookworm infection. PLoS Negl Trop Dis. 2016;10:e0004922.
Anderson AS, Trumble, BC, Hové C, Kraft TS, Kaplan H, Gurven M, Blackwell, AD. Old friends and friendly fire: Pregnancy, hookworm infection, and anemia among tropical horticulturalists. American journal of human biology : the official journal of the Human Biology Council. 2020;32(2), e23337.
Umbrello G, Pinzani R, Bandera A, et. al. Hookworm infection in infants: a case report and review of literature. Ital J Pediatr. 2021;47(26). https://doi.org/10.1186/s13052-021-00981-1
Khanh-Linh Bui, Thu-Huong Nguyen, Hieu Duc Duong, Viet-Linh Nguyen, Thi-Nhien Nguyen, Lan-Anh Le, Ha-My Cong, Khanh-Trang Tran, Duc-Vinh Le, Eiji Nagayasu, Nariaki Nonaka, Ayako Yoshida, Ancylostoma ceylanicum infections in humans in Vietnam,
Parasitology International,Volume 84, 2021, 102405,
Aula OP, McManus DP, Weerakoon KG, Olveda R, Ross AG, Rogers MJ, et al. Molecular identification of Ancylostoma ceylanicum in the Philippines. Parasitology. Cambridge University Press; 2020;147(14):1718–22.
chinapetmarket. China Pet population and ownership 2019 update [Internet]. 2020 [cited 2020 Oct 16]; Available from: https://www.chinapetmarket.com/china-pet-population-and-ownership-2019/
Jimenez Castro PD, Howell SB, Schaefer JJ, et. al. Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat?. Parasites Vectors. 2019;12(576). https://doi.org/10.1186/s13071-019-3828-6
Chung CS, Lin CK, Su KE, Liu CY, Lin CC, Liang CC, et.al. Diagnosis of Ancylostoma ceylanicum infestation by single- ballon enteroscopy (with video). Gastrointest Endosc. 2012;76(3):671-2.
Biocca F. On Ancylostoma brazillense de Faria, 1910, and Its morphological differentiation from A. ceylanicum (Looss, 1911). J Helminthol. 1951;15:1-10.
Carrall SM, Grove DI. Experimental infection of humans with Ancylostoma ceylanicum clinical, parasitological, haematological and immunological findings. Tropical and Geographical Medicine. 1968;38(1):38-45.
Areekul S, Saeaghirun C, Ukoskit K. Studies on the pathogenesis of Ancylostoma ceylanicum Blood loss in experimental dogs. Southeast Asian J Trop Med Public Health. 1975;6(2):235-40.
Rep BH, Van Joost KS, Vetter JC. Pathogenicity of Ancylostoma ceylanicum VI. Lethal blood loss in hookworm infection. Trop Geog, Med. 1971;23:184-93.
Carroll SM, Grove DI. Parasitological hematologic, and immunologic responses in acute and chronic infections of dogs with Ancylostoma ceylanicum: a model of human hookworm infection. J Infect Dis. 1984;150:284-94.
Kaya D, Yoshikawa M, Nakatani T, Tomo-oka F, Fujimoto Y, Ishida K, et al. Ancylostoma ceylanicum hookworm infection in Japanese traveler who presents chronic diarrhea after returning from Lao People’s Democratic Republic. Parasitology International 2016;65:737-40.
Yoshida Y. Comparative studies on Ancylostoma brazillense and Ancylostoma ceylanicum I. The adult stage. J Parasitol. 1971;57(5):983-9.
Yoshikawa M, Ouji Y, Hirai N, Nakamura-Uchiyama F, Yamada M, Arizono N, et al. Ancylostoma ceylanicum, novel etiological agent for traveler’s diarrhea—report of four Japanese patients who returned from Southeast Asia and Papua New Guinea. Tropical Medicine and Health. 2018;46:6-12.
Inpankaew T, Schar F, Dalsgaard A, Khieu V, Chimnoi W, Chhoun C, et al. High Prevalence of Ancylostoma ceylanicum Hookworm In Humans, Cambodia, 2012. Emerging Infectious Disease. 2014;20(6):976-82.
Conlan JV, Khamlome B, Vongxay K, Elliot A, Pallan L, Sripa B, et al. 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):624–34.
Mahdy M AK, Lim Y AL, Ngui R, Fatimah MR S, Choy SH, Y NJ, et al. Prevalence and zoonotic potential of canine hookwooks in Malaysia. Parasites and Vectors. 2012;5:88-94.
Ngui R, Lim YA L, Traub R, Mahmud R, Mistam MS. Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals. PLos Neglected Tropical Diseases. 2012;6:e1522-8.
O’Connell EM, Mitchell T, Papaiakovou M, Pilotte N, Lee D, Weinberg M, et al. Ancylostoma ceylanicum Hookworm in Myanmar Refugees, Thailand 2012-2015. Emerging Infectious Disease. 2018;24(8):1465-74.
Traub RJ, Inpankaew T, Sutthikurnchai C, Sukthana Y, Thompson RC. PCR-based coprodiagnotic tools reveal dogs as reservoirs of zoonotic ancylostomiasis Caused by Ancylostoma ceylanicum in Temple Communities in Bangkok. Vet Parasitol. 2008;155:67-73.
Phosak I, Intapan PM, Thanchomnang T, Sanpool O, Janwan P, Laummaunwai P, et al. Molecular Detection of Ancylostoma duodenale, Necator americanus in Humans in Northeastern and Southern Thailand. Korean J Parasitol. 2013; 51(6): 747-9.
Jiraanankul V, Aphijirawat W, Mungthin M, Khositnithikul R, Rangsin R, Traub RJ, et al. Incidence and Risk Factors of Hookworm Infection in a Rural Community of Central Thailand. Am J Trop Med Hyg. 2011; 84(4): 594–8.
Kladkempetch D, Tangtrongsup S, Tiwananthagorn S. Ancylostoma ceylanicum: The Neglected Zoonotic Parasite of Community Dogs in Thailand and Its Genetic Diversity among Asian Countries. Animals : an open access journal from MDPI. 2020;10(11): 2154. https://doi.org/10.3390/ani10112154
Nguyen DN, Hii SF, Nguyen VA T, Nguyen TV, Nguyen DV, Traub RJ. Re-evaluation of the species of hookworms infecting dogs in Central Vietnam. Parasites & Vectors. 2015;8:401-6.
Palmer CS, Traub RJ, Robertson ID, Hobbs RP, Elliot A, While L, et al. 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):304-13.
Smout F, Thompson RC. A, Skerratt LF. First report of Ancylostoma ceylanicum in wild canids. International Journal for Parasitology: Parasites and Wildlife. 2013;2:173-7.
Wongwigkan J, Inpankaew T. Semi-domesticated dogs as a potential reservoir for zoonotic hookworms in Bangkok, Thailand. Vet World. 2020;13(5):909-915. doi: 10.14202/vetworld.2020.909-915.
Fu Y, Huang Y, Abuzeid AM I, Hang J Prevalence and Potential Zoonotic Risk of Hookworms
From Stray Dogs and Cats in Guangdong, China. Vet Parasitol Reg Stud Reports. 2019;17: 100316.
George S, Levecke B, Kattula D, Velusamy V, Roy S, Geldhof P, et al. Molecular Identification of Hookworm Isolates in Humans, Dogs and soil in a Tribal Area in Tamil Nadu, India. PLOS Neglected Tropical Diseases. 2016;3:1-14.
Liu Y, Zheng G, Alsarakibi M, Zhang X, Hu W, Lin L, et al. The zoonotic Risk of Ancylostoma ceylanicum Isolated from Stray Dogs and Cats in Guangzhou, South China. BioMed Research International. 2014;208759.
Lui YJ, Zheng GC, Zhang P, Alsarakibi M, Zhang XH, Li YW, et al. Molecular Identification of Hookworms in stray and shelter dogs from guangzhou city, China Using ITS Sequences. J Helminthol. 2015;89(2):196-202.
Lui Y, Zheng G, Alsarakibi M, Zhang X, Hu W, Lu P, et al. Molecular Identification of Ancylostoma caninum Isolated from Cats in Southern China Based on complete ITS Sequence. BioMed Research International. 2013;868050.
Pumidonming W, Salman D, Gronsang D, AE., Sangkaeo K, Kawazu SI, Igarashi M. Prevalence of gastrointestinal helminth parasites of zoonotic significance in dogs and cats in lower Northern Thailand. J Vet Med Sci. 2016;78(12):1779–84.
Papaiakovou M, Pilotte N, Grant JR, Traub RJ, Llewelly S, McCarthy JS, et al. A novel, species-specific, real-time PCR assay for the detection of the emerging zoonotic parasite Ancylostoma ceylanicum in human stool. PLOS Neglected Tropical Diseases. 2017;11(7): e0005734
Jeerawat Saithong. Developing the potential of the network sector defensive operations helminth control [Internet]. 2021 [cited 2021 August 28] Available from: http://rbpho.moph.go.th/upload-file/doc/files/14012019-041300-1819.pdf
Alho AM, Lima C, Colella V, de Carvalho LM, Otranto D, Cardoso L. Awareness of Zoonotic Diseases and Parasite Control Practices: A Survey of Dog and Cat Owners in Qatar. Parasites & Vectors. 2018;11(1):133-9.
Saithong Jirawat. Network capacity development prevention and control of helminthiasis Rachaburi Prevention and Disease Control [Internet]. 2020 [cited 2020 Oct 16]. Available from: http://rbpho.moph.go.th/upload-file/doc/files/14012019-041300-1819.pdf
Speare R, Bradbury RS, Croese J. A case of Ancylostoma ceylanicum Infection Occuring in an Australian Soilder Returned from Solomon Islands. Korean J Parasitol. 2016;54(4):533-6.
Brunet J, Lemoine JP, Lefebvre N, Denis J, Pfaff AW, Abou-Bacar A, et al. Bloody Diarrhea Associated with Hookworm infection in Traveler Returning to France from Myanmar. Emerging Infectious Diseases. 2015;21(10):1878-9.
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