Abstract
Introduction
The animal hookworm, Ancylostoma ceylanicum, is a dominant hookworm species of dogs and cats. However, it has increasingly been found infecting humans in Southeast Asia.
Purpose
We report an autochthonous case of A. ceylanicum in a suburban area of Selangor, Malaysia. A 66-year-old Indian lady who is an avid gardener presented with chronic diarrhea of 4 months’ duration.
Methods
The patient was examined clinically and colonoscopy was performed. Adult parasites obtained via colonoscopy were subjected to microscopy and molecular investigations.
Results
Clinical examinations were unremarkable, and blood investigation revealed normochromic normocytic anemia. Stool occult blood was positive but negative for ova, cyst and adult parasites. Colonoscopy performed showed multiple diverticulae and worm infestation from the terminal ileum to sigmoid colon. Morphological examination on the adult worms showed the specific characteristics of Ancylostoma species. Molecular investigations further confirmed the nematode as Ancylostoma ceylanicum. She was treated with albendazole 400 mg daily for 3 days with symptomatic improvements sustained 3 months later. It is suspected that the patient had ingested or contacted soil contaminated with filariform larvae while gardening.
Conclusion
Information on the A. ceylanicum infection in humans, especially in urban and suburban areas, is limited, necessitating further epidemiological and clinical studies.
This is a preview of subscription content, access via your institution.
References
Traub RJ (2013) Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis. Int J Parasit 43:1009–1015. https://doi.org/10.1016/j.ijpara.2013.07.006
Inpankaew T, Schär F, Dalsgaard A, Khieu V, Chimnoi W, Chhoun C, Sok D, Marti H, Muth S, Odermatt P, Traub RJ (2014) High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012. Emerg Infect Dis 20:976–982. https://doi.org/10.3201/eid2006.131770
Yoshida Y, Okamoto K, Chiu JK (1968) Ancylostoma ceylanicum infection in dogs, cats, and man in Taiwan. Am J Trop Med Hyg 17:378–381. https://doi.org/10.4269/ajtmh.1968.17.378
Velasquez CC, Cabrera BC (1968) Ancylostoma ceylanicum (Looss, 1911) in a Filipino woman. J Parasit 54:430–431
Chowdhury AB, Schad GA (1972) Ancylostoma ceylanicum: a parasite of man in Calcutta and environs. Am J Trop Med Hyg 21:300–301. https://doi.org/10.4269/ajtmh.1972.21.300
Traub RJ, Inpankaew T, Sutthikornchai C, Sukthana Y, Thompson RA (2008) PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in Bangkok. Vet Parasit 155:67–73. https://doi.org/10.1016/j.vetpar.2008.05.001
Aung WPP, Htoon TT, Tin HH, Sanpool O, Jongthawin J, Sadaow L, Phosuk I, Ropai R, Intapan PM, Maleewong W (2017) First molecular identifications of Necator americanus and Ancylostoma ceylanicum infecting rural communities in lower Myanmar. Am J Trop Med Hyg 96:214–216. https://doi.org/10.4269/ajtmh.16-0610
O’Connell EM, Mitchell T, Papaiakovou M, Pilotte N, Lee D, Weinberg M, Sakulrak P, Tongsukh D, Oduro-Boateng G, Harrison S, Williams SA (2018) Ancylostoma ceylanicum Hookworm in Myanmar Refugees, Thailand, 2012–2015. Emerg Infect Dis 24:1472–1478. https://doi.org/10.3201/eid2408.180280
Smout FA, Skerratt LF, Butler JR, Johnson CN, Congdon BC, Thompson RA (2017) The hookworm Ancylostoma ceylanicum: An emerging public health risk in Australian tropical rainforests and Indigenous communities. One Health 3:66–69. https://doi.org/10.1016/j.onehlt.2017.04.002
Bradbury RS, Hii SF, Harrington H, Speare R, Traub R (2017) Ancylostoma ceylanicum hookworm in the Solomon Islands. Emerg Infect Dis 23:252–257. https://doi.org/10.3201/eid2302.160822
Norhayati M, Fatmah MS, Yusof S, Edariah AB (2003) Intestinal parasitic infections in man: a review. Med J Malaysia 58:296–305
Ngui R, Aziz S, Chua KH, Aidil RM, Lee SC, Tan TK, Sani MM, Arine AF, Rohela M, Lim YA (2015) Patterns and risk factors of soil-transmitted helminthiasis among orang Asli subgroups in peninsular Malaysia. Am J Trop Med Hyg 93:361–370. https://doi.org/10.4269/ajtmh.13-0677
Ngui R, Lee SC, Tan TK, Roslan MA, Lim YAL (2012) Molecular identification of human hookworm infections in economically disadvantaged communities in Peninsular Malaysia. Am J Trop Med Hyg 86:837–842. https://doi.org/10.4269/ajtmh.2012.11-0446
Ngui R, Lim YAL, Traub R, Mahmud R, Mistam MS (2012) Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals. PLoS Negl Trop Dis 6:e1522. https://doi.org/10.1371/journal.pntd.0001522
Jamaiah I, Rohela M (2005) Prevalence of intestinal parasites among members of the public in Kuala Lumpur, Malaysia. Southeast Asian J Trop Med Public Health 36:68–71
Asady, Ismail S, Jalil MA, Pakeer O (2019). Soil transmitted helminth infection among children admitted to Hospital Tengku Ampuan Afzan, Kuantan, Pahang. IIUM Med J Malaysia 18(2). https://journals.iium.edu.my/kom/index.php/imjm/article/view/89
Ngui R, Lee SC, Tan TK, Muhammad Aidil R, Lim YAL (2012) Genetic characterization of human hookworm infections in rural and remote areas of Peninsular Malaysia. Am J Trop Med Hyg 86:837–842. https://doi.org/10.4269/ajtmh.2012.11-0446
Conlan JV, Sripa B, Attwood S, Newton PN (2011) A review of parasitic zoonoses in a changing Southeast Asia. Vet Parasit 182:22–40. https://doi.org/10.1016/j.vetpar.2011.07.013
Conlan JV, Khamlome B, Vongxay K, Elliot A, Pallant L, Sripa B, Blacksell SD, Fenwick S, Thompson RC (2012) Soil-transmitted helminthiasis in Lao People’s Democratic Republic: a community-wide cross-sectional study of humans and dogs in a mass drug administration environment. Am J Trop Med Hyg 86:624–634. https://doi.org/10.4269/ajtmh.2012.11-0413
Arebkul S, Radomyos P, Viravan C (1970) Experimental infection of Ancylostoma ceylanicum in man. J Med Assoc Thailand 53:190–194
Yoshida Y, Okamoto K, Chiu JK (1971) Experimental infection of man with Ancylostoma ceylanicum Looss. 1911. Chinese J Microbiol 4:157–167
Thompson RCA (2015) Neglected zoonotic helminths: Hymenolepis nana, Echinococcus canadensis and Ancylostoma ceylanicum. Clin Microbiol Infect 21:426–432. https://doi.org/10.1016/j.cmi.2015.01.004
Ngui R, Mahdy MA, Chua KH, Traub R, Lim YAL (2013) 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 128:154–157. https://doi.org/10.1016/j.actatropica.2013.06.003
Papaiakovou M, Pilotte N, Grant JR, Traub RJ, Llewellyn S, McCarthy JS, Krolewiecki AJ, Cimino R, Mejia R, Williams SA (2017) A novel, species-specific, real-time PCR assay for the detection of the emerging zoonotic parasite Ancylostoma ceylanicum in human stool. PLoS Negl Trop Dis 11:e0005734. https://doi.org/10.1371/journal.pntd.0005734
Ngui R, Lim YAL, Ismail WHW, Lim KN, Mahmud R (2014) Zoonotic Ancylostoma ceylanicum infection detected by endoscopy. Am J Trop Med Hyg 91:86–88. https://doi.org/10.4269/ajtmh.13-0756
Kaya D et al (2016) Ancylostoma ceylanicum hookworm infection in Japanese traveler who presented chronic diarrhea after return from Lao People’s Democratic Republic. Parasitol Int 65:737–740. https://doi.org/10.1016/j.parint.2016.07.001
Yoshikawa M, Ouji Y, Hirai N, Nakamura-Uchiyama F, Yamada M, Arizono N, Akamatsu N, Yoh T, Kaya D, Nakatani T, Kikuchi E (2018) Ancylostoma ceylanicum, novel etiological agent for traveler’s diarrhea—report of four Japanese patients who returned from Southeast Asia and Papua New Guinea. Trop Med Health 46:1–6. https://doi.org/10.1186/s41182-018-0087-8
Sahimin N, Lim YAL, Douadi B, Khalid MKNM, Wilson JJ, Behnke JM, Zain SNM (2017) Hookworm infections among migrant workers in Malaysia: molecular identification of Necator americanus and Ancylostoma duodenale. Acta Trop 173:109–115. https://doi.org/10.1016/j.actatropica.2017.06.011
Yoshida Y, Okamoto K, Matsuo K, Kwo EH, Retnasaba-Pathy A (1973) The occurrence of Ancylostoma braziliense (de Faria, 1910) and Ancylostoma ceylanicum (Looss, 1911) in Malaysia. Southeast Asian J Trop Med Public Health 4:498–503
Mahdy MA, Lim YAL, Ngui R, Fatimah MS, Choy SH, Yap NJ, Al-Mekhlafi HM, Ibrahim J, Surin J (2012) Prevalence and zoonotic potential of canine hookworms in Malaysia. Parasites Vectors 5:88. https://doi.org/10.1186/1756-3305-5-88
Tun S, Ithoi I, Mahmud R, Samsudin NI, Heng CK, Ling LY (2015) Detection of helminth eggs and identification of hookworm species in stray cats, dogs and soil from Klang Valley. Malaysia PloS One 10:e0142231. https://doi.org/10.1371/journal.pone.0142231
Hsu YC, Lin JT (2012) Intestinal infestation with Ancylostoma ceylanicum. N Engl J Med 366:e20. https://doi.org/10.1056/NEJMicm1101717
Zajíčková M, Nguyen LT, Skálová L, Stuchlíková LR, Matoušková P (2019) Anthelmintics in the future: current trends in the discovery and development of new drugs against gastrointestinal nematodes. Drug Discov Today 25:430–437. https://doi.org/10.1016/j.drudis.2019.12.007
Wiśniewski M, Łapiński M, Daniłowicz-Luebert E, Jaros S, Długosz E, Wędrychowicz H (2016) Vaccination with a cocktail of Ancylostoma ceylanicum recombinant antigens leads to worm burden reduction in hamsters. Acta Parasitol 61:556–561. https://doi.org/10.1515/ap-2016-0074
Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993. https://doi.org/10.1038/nature06536
Jung BK, Lee JY, Chang T, Song H, Chai JY (2020) Rare case of enteric Ancylostoma caninum hookworm infection, South Korea. Emerg Infect Dis 26:181–183. https://doi.org/10.3201/eid2601.191335
Stracke K, Jex AR, Traub RJ (2020) Zoonotic ancylostomiasis: an update of a continually neglected zoonosis. Am J Trop Med Hyg. https://doi.org/10.4269/ajtmh.20-0060
Acknowledgements
We thank the staff at the Gastroenterology Unit and Microbiology Laboratory, Clinical Trial Centre, Faculty of Medicine, UiTM for their kind support and assistance.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
Writing and identification of the worms: CCH; extracting worms via colonoscopy from patient: ARR; molecular identification of the worms: RN.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethical Approval
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Heo, C.C., Rafiz, A.R. & Ngui, R. A Case of Zoonotic Ancylostoma ceylanicum Infection in a Suburban Area of Selangor, Malaysia. Acta Parasit. 67, 564–568 (2022). https://doi.org/10.1007/s11686-021-00478-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11686-021-00478-1
Keywords
- Zoonotic hookworm
- Ancyclostoma
- Ceylanicum
- Colonoscopy
- Ancylostomiasis
- Malaysia