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Molecular identification of Ancylostoma ceylanicum in the Philippines

Published online by Cambridge University Press:  24 August 2020

Oyime P. Aula Open the ORCID record for Oyime P. Aula [Opens in a new window] ,
Donald P. McManus Open the ORCID record for Donald P. McManus [Opens in a new window] ,
Kosala G. Weerakoon ,
Remigio Olveda ,
Allen G. Ross ,
Madeleine J. Rogers  and
Catherine A. Gordon Open the ORCID record for Catherine A. Gordon [Opens in a new window]
Oyime P. Aula
Affiliation:
Molecular Parasitology Laboratory, QIMR Berghofer Medical Research Institute, Queensland, Australia School of Chemistry and Molecular Biology, The University of Queensland, Queensland, Australia
Donald P. McManus
Affiliation:
Molecular Parasitology Laboratory, QIMR Berghofer Medical Research Institute, Queensland, Australia
Kosala G. Weerakoon
Affiliation:
Department of Parasitology, Faculty of Medicine and Allied Sciences, Rajarata University of Sri Lanka, Sri Lanka
Remigio Olveda
Affiliation:
Immunology Department, Research Institute of Tropical Medicine, Manila, the Philippines
Allen G. Ross
Affiliation:
Menzies Health Institute Queensland, Gold Coast, Australia icddr b, Dhaka, Bangladesh
Madeleine J. Rogers
Affiliation:
Molecular Parasitology Laboratory, QIMR Berghofer Medical Research Institute, Queensland, Australia School of Chemistry and Molecular Biology, The University of Queensland, Queensland, Australia
Catherine A. Gordon*
Affiliation:
Molecular Parasitology Laboratory, QIMR Berghofer Medical Research Institute, Queensland, Australia
*
Author for correspondence: Catherine A. Gordon, E-mail: Catherine.Gordon@qimrberghofer.edu.au
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Abstract

Hookworms are some of the most widespread of the soil-transmitted helminths (STH) with an estimated 438.9 million people infected. Until relatively recently Ancylostoma ceylanicum was regarded as a rare cause of hookworm infection in humans, with little public health relevance. However, recent advances in molecular diagnostics have revealed a much higher prevalence of this zoonotic hookworm than previously thought, particularly in Asia. This study examined the prevalence of STH and A. ceylanicum in the municipalities of Palapag and Laoang in the Philippines utilizing real-time polymerase chain reaction (PCR) on stool samples previously collected as part of a cross-sectional survey of schistosomiasis japonica. Prevalence of hookworm in humans was high with 52.8% (n = 228/432) individuals positive for any hookworm, 34.5% (n = 149/432) infected with Necator americanus, and 29.6% (n = 128/432) with Ancylostoma spp; of these, 34 were PCR-positive for A. ceylanicum. Considering dogs, 12 (n = 33) were PCR-positive for A. ceylanicum. This is the first study to utilize molecular diagnostics to identify A. ceylanicum in the Philippines with both humans and dogs infected. Control and elimination of this zoonotic hookworm will require a multifaceted approach including chemotherapy of humans, identification of animal reservoirs, improvements in health infrastructure, and health education to help prevent infection.

Keywords

Ancylostoma ceylanicumAncylostoma duodenaleNecator americanusPhilippinesreal-time PCR
Type
Research Article
Information
Parasitology , Volume 147 , Issue 14 , December 2020 , pp. 1718 - 1722
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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Footnotes

†

Deceased 2020

References

Basuni, M, Muhi, J, Othman, N, Verweij, JJ, Ahmad, M, Miswan, N, Rahumatullah, A, Aziz, FA, Zainudin, NS and Noordin, R (2011) A pentaplex real-time polymerase chain reaction assay for detection of four species of soil-transmitted helminths. American Journal of Tropical Medicine and Hygiene 84, 338–343.CrossRefGoogle ScholarPubMed
Bethony, J, Brooker, S, Alboico, M, Geirger, SM, Loukas, A, Diemart, D and Hotez, PJ (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. The Lancet 367, 1521–1532.10.1016/S0140-6736(06)68653-4CrossRefGoogle ScholarPubMed
Bradbury, R and Traub, RJ (2016) Hookworm Infection in Oceania. In Loukas, A (ed.), Neglected Tropical Diseases – Oceania. Cham: Springer International Publishing, pp. 33–68.CrossRefGoogle Scholar
Bradbury, RS, Hii, SF, Harrington, H, Speare, R and Traub, R (2017) Ancylostoma ceylanicum hookworm in the Solomon Islands. Emerging Infectious Diseases 23, 252–257.CrossRefGoogle ScholarPubMed
Conlan, JV, Khamlome, B, Vongxay, K, Elliot, A, Pallant, L, Sripa, B, Blacksell, SD, Fenwick, S and Thompson, RC (2012) Soil-transmitted helminthiasis in Laos: a community-wide cross-sectional study of humans and dogs in a mass drug administration environment. American Journal of Tropical Medicine and Hygiene 86, 624–634.CrossRefGoogle Scholar
DepED (2015 a) Implementation of the national school deworming day. In Education (ed.), Division Memorandum. Bohol, the Philippines: DepED, pp. 1–20.Google Scholar
DepED (2015 b) Second round of national school deworming Day for school year 2015–2016. In Education (ed.), Division Memorandum. The Philippines: DepED, pp. 1–2.Google Scholar
DepED (2016) DOH conducts national deworming month to reinforce prevention and control of soil-transmitted helminths. Vol. 2020.Google Scholar
de Silva, NR, Brooker, S, Hotez, PJ, Montresor, A, Engels, D and Savioli, L (2003) Soil-transmitted helminth infections: updating the global picture. Trends in Parasitology 19, 547–551.10.1016/j.pt.2003.10.002CrossRefGoogle ScholarPubMed
Gordon, CA, Acosta, LP, Gobert, GN, Jiz, M, Olveda, RM, Ross, AG, Gray, DJ, Williams, GM, Harn, D, Yuesheng, L and McManus, DP (2015 a) High prevalence of Schistosoma japonicum And Fasciola Gigantica In bovines from Northern Samar, the Philippines. PLoS Neglected Tropical Diseases 9, e0003108.10.1371/journal.pntd.0003108CrossRefGoogle ScholarPubMed
Gordon, CA, Acosta, LP, Gobert, GN, Olveda, RM, Ross, AG, Williams, GM, Gray, DJ, Harn, D, Li, Y and McManus, DP (2015 b) Real-time PCR demonstrates high prevalence of Schistosoma japonicum in the Philippines: implications for surveillance and control. PLoS Neglected Tropical Diseases 9, e0003483.10.1371/journal.pntd.0003483CrossRefGoogle ScholarPubMed
Gordon, CA, McManus, DP, Acosta, LP, Olveda, R, Williams, M, Ross, AG, Gray, DJ and Gobert, GN (2015 c) Multiplex real-time PCR monitoring of intestinal helminths in humans reveals widespread polyparasitism in Northern Samar, the Philippines. International Journal for Parasitology 45, 477–483.10.1016/j.ijpara.2015.02.011CrossRefGoogle ScholarPubMed
Inobaya, MT, Chau, TN, Ng, S-K, MacDougall, C, Olveda, RM, Tallo, VL, Landicho, JM, Malacad, CM, Aligato, MF, Guevarra, JB and Ross, AG (2018) Mass drug administration and the sustainable control of schistosomiasis: an evaluation of treatment compliance in the rural Philippines. Parasites and Vectors 11, 441.10.1186/s13071-018-3022-2CrossRefGoogle ScholarPubMed
Inpankaew, T, Schar, F, Dalsgaard, A, Khieu, V, Chimnoi, W, Chhoun, C, Sok, D, Marti, H, Muth, S, Odermatt, P and Traub, RJ (2014) High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012. Emerging Infectious Diseases 20, 976–982.CrossRefGoogle ScholarPubMed
Jiraanankul, V, Aphijirawat, W, Mungthin, M, Khositnithikul, R, Rangsin, R, Traub, RJ, Piyaraj, P, Naaglor, T, Taamasri, P and Leelayoova, S (2011) Incidence and risk factors of hookworm infection in a rural community of central Thailand. American Journal of Tropical Medicine and Hygiene 84, 594–598.10.4269/ajtmh.2011.10-0189CrossRefGoogle Scholar
Ngui, R, Ching, LS, Kai, TT, Roslan, MA and Lim, YA (2012 a) Molecular identification of human hookworm infections in economically disadvantaged communities in Peninsular Malaysia. American Journal of Tropical Medicine and Hygiene 86, 837–842.10.4269/ajtmh.2012.11-0446CrossRefGoogle ScholarPubMed
Ngui, R, Lim, YA, Traub, R, Mahmud, R and Mistam, MS (2012 b) Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals. PLoS Neglected Tropical Diseases 6, e1522.CrossRefGoogle ScholarPubMed
Ngui, R, Mahdy, MA, Chua, KH, Traub, R and Lim, YA (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 Tropica 128, 154–157.10.1016/j.actatropica.2013.06.003CrossRefGoogle ScholarPubMed
Ngui, R, Lim, YA, Ismail, WH, Lim, KN and Mahmud, R (2014) Zoonotic Ancylostoma ceylanicum infection detected by endoscopy. American Journal of Tropical Medicine and Hygiene 91, 86–88.CrossRefGoogle ScholarPubMed
Olveda, DU, Olveda, RM, Lam, AK, Chau, TN, Li, Y, Gisparil, AD, 2nd and Ross, AG (2014) Utility of diagnostic imaging in the diagnosis and management of schistosomiasis. Clinical Microbiology (Los Angeles, Calif), 3, 142.Google ScholarPubMed
Olveda, DU, Inobaya, M, McManus, DP, Olveda, RM, Vinluan, ML, Ng, SK, Harn, DA, Li, Y, Guevarra, JR, Lam, AK and Ross, AG (2016) Biennial versus annual treatment for schistosomiasis and its impact on liver morbidity. International Journal of Infectious Diseases 54, 145–149.CrossRefGoogle ScholarPubMed
Palmer, CS, Traub, RJ, Robertson, ID, Hobbs, RP, Elliot, A, While, L, Rees, R and Thompson, RCA (2007) The veterinary and public health significance of hookworm in dogs and cats in Australia and the status of A. ceylanicum. Veterinary Parasitology, 145, 304–313.10.1016/j.vetpar.2006.12.018CrossRefGoogle ScholarPubMed
Papaiakovou, M, Pilotte, N, Grant, JR, Traub, RJ, Llewellyn, S, McCarthy, JS, Krolewiecki, AJ, Cimino, r, Mejia, R and 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 Neglected Tropical Diseases 11, e0005734.CrossRefGoogle ScholarPubMed
Papier, K, Williams, GM, Luceres-Catubig, R, Ahmed, F, Olveda, RM, McManus, DP, Chy, D, Chau, TN, Gray, DJ and Ross, AG (2014) Childhood malnutrition and parasitic helminth interactions. Clinical Infectious Diseases 59, 234–243.CrossRefGoogle ScholarPubMed
Peñas, JA, de Los Reyes, VC, Sucaldito, MNL, Ballera, JED, Hizon, HL, Magpantay, RL, Belizario, VY Jr and Hartigan-Go, K (2018) Epidemic hysteria following the national school deworming Day, Zamboanga Peninsula, Philippines, 2015. Western Pacific Surveillance and Response Journal, 9, 1-6.10.5365/wpsar.2017.8.1.009CrossRefGoogle ScholarPubMed
Pilotte, N, Papaiakovou, M, Grant, JR, Bierwert, LA, Llewellyn, S, McCarthy, JS and Williams, SA (2016) Improved PCR-based detection of soil transmitted helminth infections using a next-generation sequencing approach to assay design. PLOS Neglected Tropical Diseases 10, e0004578.CrossRefGoogle ScholarPubMed
Pullan, RL, Bethony, JM, Geiger, SM, Correa-Oliveira, R, Brooker, S and Quinnell, RJ (2010) Human helminth co-infection: no evidence of common genetic control of hookworm and Schistosoma mansoni infection intensity in a Brazilian community. International Journal for Parasitology, 40, 299–306.CrossRefGoogle Scholar
Ross, A, Olveda, R, Olveda, D, Harn, D, Gray, DJ, McManus, DP, Tallo, V, Chau, T and Williams, G (2015) Can mass drug administration lead to the sustainable control of schistosomiasis in the Philippines? The Journal of Infectious Diseases 211, 283–289.CrossRefGoogle Scholar
Ross, AG, Papier, K, Luceres-Catubig, R, Chau, TN, Inobaya, MT and Ng, SK (2017) Poverty, dietary intake, intestinal parasites, and nutritional status among school-age children in the rural Philippines. Tropical Medicine & Infectious Disease 2, 49.CrossRefGoogle ScholarPubMed
Setasuban, P, Vajrasthira, S and Muennoo, C (1976) Prevalence and zoonotic potential of Ancylostoma ceylanicum in cats in Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 7, 534–539.Google ScholarPubMed
Taniuchi, M, Verweij, JJ, Noor, Z, Sobuz, SU, Lieshout, L, Petri, WA, Haque, R and Houpt, ER (2011) High throughput multiplex PCR and Probe-based detection with luminex beads for seven intestinal parasites. American Journal of Tropical Medicine and Hygiene 84, 332–337.CrossRefGoogle ScholarPubMed
Traub, RJ (2013) Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis. International Journal for Parasitology 43, 1009–1015.10.1016/j.ijpara.2013.07.006CrossRefGoogle ScholarPubMed
Traub, RJ, Inpankaew, T, Sutthikornchai, C, Sukthana, Y and Thompson, RCA (2008) PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in Bangkok. Veterinary Parasitology 155, 67–73.10.1016/j.vetpar.2008.05.001CrossRefGoogle ScholarPubMed
Velasquez, CC and Cabrera, BC (1968) Ancylostoma ceylanicum (Looss, 1911) in a Filipino woman. Journal of Parasitology 54, 430–431.10.2307/3277059CrossRefGoogle Scholar
Weerakoon, KG, Gordon, CA, Williams, GM, Cai, P, Gobert, GN, Olveda, RM, Ross, AG, Olveda, DU and McManus, DP (2017) Droplet digital PCR diagnosis of human schistosomiasis: parasite cell-free DNA detection in diverse clinical samples. Journal of Infectious Diseases 216, 1611–1622.CrossRefGoogle ScholarPubMed
Weerakoon, KG, Gordon, CA, Williams, GM, Cai, P, Gobert, GN, Olveda, RM, Ross, AG, Olveda, DU and McManus, DP (2018) Co-parasitism of intestinal protozoa and Schistosoma japonicum in a rural community in the Philippines. Infectious Diseases of Poverty 7, 121.CrossRefGoogle Scholar
Yoshida, Y, Okamoto, K and Chiu, JK (1968) Ancylostoma ceylanicum infection in dogs, cats, and man in Taiwan. American Journal of Tropical Medicine and Hygiene 17, 378–381.10.4269/ajtmh.1968.17.378CrossRefGoogle ScholarPubMed
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