Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis

International Journal for Parasitology

Volumn 43, Issue 12-13, 2013, Pages 1009-1015

  Traub, Rebecca J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Ancylostoma ceylanicum; Emerging disease; Hookworm; Zoonosis

Indexed keywords

ADVANTAGE; ADVOCATE; DRONTAL; DRONTAL PLUS; EMODEPSIDE; EMODEPSIDE PLUS PRAZIQUANTEL; FEBANTEL; IMIDACLOPRID; IVERMECTIN; MOXIDECTIN; PRAZIQUANTEL; PYRANTEL; UNCLASSIFIED DRUG;

ALLERGY; HEALTH RISK; MOLECULAR ANALYSIS; MORBIDITY; NEMATODE; PATHOLOGY; PUBLIC HEALTH;

ANCYLOSTOMA CEYLANICUM; ANCYLOSTOMIASIS; ANEMIA; ENVIRONMENTAL SANITATION; GEOGRAPHIC DISTRIBUTION; HOOKWORM INFECTION; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; INFECTION CONTROL; LIFE CYCLE; MIXED INFECTION; NECATORIASIS; NONHUMAN; PARASITE IDENTIFICATION; PARASITE TRANSMISSION; PARASITE VIRULENCE; PATHOGENESIS; REVIEW;

ASIA;

ANCYLOSTOMA CANINUM; ANCYLOSTOMA CEYLANICUM; ANCYLOSTOMATOIDEA; CANIS FAMILIARIS;

ANCYLOSTOMA CEYLANICUM; EMERGING DISEASE; HOOKWORM; ZOONOSIS;

ANCYLOSTOMA; ANCYLOSTOMIASIS; ANIMALS; ASIA; COMMUNICABLE DISEASES, EMERGING; HUMANS; ZOONOSES;

EID: 84884702758     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2013.07.006     Document Type: Review

References (85)

1. Amin-Babjee Parasites of the domestic cat in Selangor, Malaysia. Kajian Vet. 1978, 10:107-114.
2. Anten J.F., Zuidema P.J. Hookworm infection in Dutch servicemen returning from West New Guinea. Trop. Geog. Med. 1964, 64:216-224.
3. Areekul S., Radomyos P., Viravan C. Experimental infection of Ancylostoma ceylanicum in man. J. Med. Assoc. Thai 1970, 53:190-194.
4. Areekul S., Radomyos P., Viravan C. Preliminary report of Ancylostoma ceylanicum infection in Thai people. J. Med. Assoc. Thai. 1970, 53:315-321.
5. 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, 6:235-240.
6. Areekul S., Viravan C., Radomyos P. Experimental infection of A. ceylanicum by oral route in man. Southeast Asian J. Trop. Med. Public Health 1973, 4:138.
7. Baker M.K., Lange L., Verster A., van der Plaat S. A survey of helminths in domestic cats in the Pretoria area of Transvaal, Republic of South Africa. Part 1: The prevalence and comparison of burdens of helminths in adult and juvenile cats. J. S. Afr. Vet. Assoc. 1989, 60:139-142.
8. Baltz J.G., Mishra R., Yeaton P. Unusual case of hookworm presenting as acute surgical abdomen. Am. J. Med. 2009, 122:e3-4.
9. Barakat M., Ibrahim N., Nasr A. In vivo endoscopic imaging of ancylostomiasis-induced gastrointestinal bleeding: clinical and biological profiles. Am. J. Trop. Med. Hyg. 2012, 87:701-705.
10. Behnke J.M., Rose R., Garside P. Sensitivity to ivermectin and pyrantel of Ancylostoma ceylanicum and Necator americanus. Int. J. Parasitol. 1993, 23:945-952.
11. Behnke J.M., Rose R., Little J. Resistance of the hookworms Ancylostoma ceylanicum and Necator americanus to intestinal inflammatory responses induced by heterologous infection. Int. J. Parasitol. 1994, 24:91-101.
12. Behnke J., Guest J., Rose R. Expression of acquired immunity to the hookworm Ancylostoma ceylanicum in hamsters. Parasite Immunol. 1997, 19:309-318.
13. Bethony J., Brooker S., Albonico M., Geiger S.M., Loukas A., Diemert D., Hotez P.J. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 2006, 367:1521-1532.
14. Biocca E. On Ancylostoma braziliense (de Faria, 1910) and its morphological differentiation from A. ceylanicum (Looss, 1911). J. Helminthol. 1951, 15:1-10.
15. Bonne C. Invasion of the submucosa of the human small intestine by Ancylostoma braziliense. Am. J. Trop. Med. 1937, 17:587-594.
16. Bonne C. Invasion of the human intestinal wall by ancylostomes. Am. J. Trop. Med. Hyg. 1942, 22:507-509.
17. Carroll S.M., Grove D.I. 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, 150:284-294.
18. Carroll S.M., Grove D.I. Experimental infection of humans with Ancylostoma ceylanicum: clinical, parasitological, haematological and immunological findings. Trop. Geog. Med. 1986, 38:38-45.
19. Chen J., Xu M.J., Zhou D.H., Song H.Q., Wang C.R., Zhu X.Q. Canine and feline parasitic zoonoses in China. Parasite Vectors 2012, 5:152.
20. Chen Y.Y., Soon M.S. Endoscopic diagnosis of hookworm infection that caused intestinal bleeding. Gastrointest. Endosc. 2005, 62:142.
21. Chowdhury A.B., Schad G.A. Ancylostoma ceylanicum: a parasite of man in Calcutta and environs. Am. J. Trop. Med. Hyg. 1972, 21:300-301.
22. Chung C.S., Lin C.K., Su K.E., Liu C.Y., Lin C.C., Liang C.C., Lee T.H. Diagnosis of Ancylostoma ceylanicum infestation by single-balloon enteroscopy (with video). Gastrointest. Endosc. 2012, 76:671-672.
23. Conlan J.V., Khamlome B., Vongxay K., Elliot A., Pallant L., Sripa B., Blacksell S.D., Fenwick S., Thompson R.C. 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, 86:624-634.
24. Constable S.E., Dixon R.M., Dixon R.J., Toribio J.A. Approaches to dog health education programs in Australian rural and remote indigenous communities: four case studies. Health Promot. Int. 2012, 28:322-332.
25. Croese J., Loukas A., Opdebeeck J., Fairley S., Prociv P. Human enteric infection with canine hookworms. Ann. Intern. Med. 1994, 120:369-374.
26. Croese J., Speare R. Intestinal allergy expels hookworms: seeing is believing. Trends Parasitol. 2006, 22:547-550.
27. Croese J., Wood M.J., Melrose W., Speare R. Allergy controls the population density of Necator americanus in the small intestine. Gastroenterology 2006, 131:402-409.
28. Crompton D.W. The public health importance of hookworm disease. Parasitology 2000, 121:S39-S50.
29. Darling S. Ancylostoma braziliense de Faria, 1910, and its occurrence in man and animals. Am. J. Hyg. 1924, 4:416-448.
30. Dissanaike A.S. On some helminths of dogs in Colombo and their bearing on human infections, with a description of a new trematode Heterophysopsis yehi sp. nov. (Heterphyidae). Ceylon J. Med. Sci. 1961, 10:1-12.
31. Gordon E. Ancylostomes recorded from sixty-seven post mortems performed in Amazonas, Brazil. Ann. Trop. Med. Parasitol. 1922, 16:223-228.
32. Haydon G., Bearup A. Correspondence: Ancylostoma braziliense and Ancylostoma ceylanicum. Trans. R. Soc. Trop. Med. Hyg. 1963, 57:76.
33. Horton J. Global anthelmintic chemotherapy programs: learning from history. Trends Parasitol. 2003, 19:405-409.
34. Hoskins J.D., Malone J.B., Smith P.H. Prevalence of parasitism diagnosed by fecal examination in Louisiana dogs. Am. J. Vet. Res. 1982, 43:1106-1109.
35. Hsu Y.C., Lin J.T. Images in clinical medicine. Intestinal infestation with Ancylostoma ceylanicum. N. Engl. J. Med. 2012, 366:e20.
36. Inpankaew T., Traub R., Thompson R.C., Sukthana Y. Canine parasitic zoonoses in Bangkok temples. Southeast Asian J. Trop. Med. Public Health 2007, 38:247-255.
37. Jex A.R., Lim Y.A., Bethony J.M., Hotez P.J., Young N.D., Gasser R.B. Soil-transmitted helminths of humans in Southeast Asia-towards integrated control. Adv. Parasitol. 2011, 74:231-265.
38. Jiraanankul V., Aphijirawat W., Mungthin M., Khositnithikul R., Rangsin R., Traub R.J., Piyaraj P., Naaglor T., Taamasri P., Leelayoova S. Incidence and risk factors of hookworm infection in a rural community of central Thailand. Am. J. Trop. Med. Hyg. 2011, 84:594-598.
39. Koehler A.V., Bradbury R.S., Stevens M.A., Haydon S.R., Jex A.R., Gasser R.B. Genetic characterization of selected parasites from people with histories of gastrointestinal disorders using a mutation scanning coupled approach. Electrophoresis 2013, 34:1720-1728.
40. Kshaunish D., Kausik D., Dasgupta J., Dhali G.K., Chowdhury A. Hookworm infection presenting as overt gastrointestinal bleeding: lessons from double-balloon enteroscopy in the tropics. Am. J. Gastroenterol. 2008, 103:1310-1311.
41. Lane H.C. Ancylostoma ceylanicum, a new human parasite. Indian Med. Gazette 1913, 48:216-218.
42. Looss A. The anatomy and life history of Agchlostoma duodenale, Dubini. Records of the School of Medicine. Egypt Ministry of Education, Cairo 1911, 4:531-536.
43. Mahadeva S., Qua C.S., Yusoff W., Sulaiman W. Repeat endoscopy for recurrent iron deficiency anemia: an (un)expected finding from southeast Asia. Dig. Dis. Sci. 2007, 52:523-525.
44. Maplestone P. Creeping eruption produced by hookworm larvae. Indian Med. Gazette 1933, 68:251.
45. Margono S.S., Koesharjono C., Kosin E. Hookworm in dogs and cats in the area of Jakarta. Trop. Geog. Med. 1979, 31:257-261.
46. Miller T.A. Blood loss during hookworm infection, determined by erythrocyte labeling with radioactive 51-chromium. II. Pathogenesis of Ancylostoma braziliense infection in dogs and cats. J. Parasitol. 1966, 52:856-865.
47. Miller T.A. Pathogenesis and immunity in hookworm infection. Trans. R. Soc. Trop. Med. Hyg. 1968, 62:473-489.
48. Miller T.A. Hookworm infection in man. Adv. Parasitol. 1979, 17:315-384.
49. Mohamed A.S., Moore G.E., Glickman L.T. Prevalence of intestinal nematode parasitism among pet dogs in the United States (2003-2006). J. Am. Vet. Med. Assoc. 2009, 234:631-637.
50. Ngui R., Lim Y.A., Traub R., Mahmud R., Mistam M.S. Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals. PLoS Negl. Trop. Dis. 2012, 6:e1522.
51. Palmer C.S., Traub R.J., Robertson I.D., Hobbs R.P., Elliot A., While L., Rees R., Thompson R.C. The veterinary and public health significance of hookworm in dogs and cats in Australia and the status of A. ceylanicum. Vet. Parasitol. 2007, 145:304-313.
52. Paterson S., Viney M.E. Host immune responses are necessary for density dependence in nematode infections. Parasitology 2002, 125:283-292.
53. Ray D.K., Bhopale K.K., Shrivastava V.B. Migration and growth of Ancylostoma ceylanicum in golden hamsters Mesocricetus auratus. J. Helminthol. 1972, 46:357-362.
54. Rep B.H., Heinemann D.W. Changes in hookworm distribution in Surinam. Trop. Geog. Med. 1976, 28:104-110.
55. Rep B.H., van Joost K.S., Vetter J.C. Pathogenicity of Ancylostoma ceylanicum. VI. Lethal blood loss in hookworm infection. Trop. Geog. Med. 1971, 23:184-193.
56. Rep B.H., Vetter J.C.M., Eijsker M. Cross breeding experiments in Ancylostoma braziliense de Faria, 1910 and A. ceylanicum Looss, 1911. Trop. Geog. Med. 1968, 20:367-378.
57. Ricci N.D., Fiuza J.A., Bueno L.L., Cancado G.G.L., Gazzinelli-Guimaraes P.H. Induction of CD4+CD25+FOXP3+ Regulatory T Cells during human hookworm infection modulates antigen-mediated lymphocyte proliferation. PLoS Negl. Trop. Dis. 2011, 5:e1383. 10.1371/journal.pntd.0001383.
58. Roche M., Layrisse M. The nature and causes of "hookworm anemia". Am. J. Trop. Med. Hyg. 1966, 15:1029-1102.
59. Sato M., Sanguankiat S., Yoonuan T., Pongvongsa T., Keomoungkhoun M., Phimmayoi I., Boupa B., Moji K., Waikagul J. Copro-molecular identification of infections with hookworm eggs in rural Lao PDR. Trans. R. Soc. Trop. Med. Hyg. 2010, 104:617-622.
60. Scholz T., Uhlirova M., Ditrich O. Helminth parasites of cats from the Vientiane province, Laos, as indicators of the occurrence of causative agents of human parasitoses. Parasite 2003, 10:343-350.
61. Schuster R.K., Thomas K., Sivakumar S., O'Donovan D. The parasite fauna of stray domestic cats (Felis catus) in Dubai, United Arab Emirates. Parasitol. Res. 2009, 105:125-134.
62. Setasuban P., Vajrasthira S., Muennoo C. Prevalence and zoonotic potential of Ancylostoma ceylanicum in cats in Thailand. Southeast Asian J. Trop. Med. Public Health 1976, 7:534-539.
63. Taweethavonsawat P., Chungpivat S., Satranarakun P., Traub R.J., Schaper R. Efficacy of a combination product containing pyrantel, febantel and praziquantel (Drontal Plus Flavour, Bayer Animal Health) against experimental infection with the hookworm Ancylostoma ceylanicum in dogs. Parasitol. Res. 2009, 106:533-537.
64. Taweethavonsawat P., Chungpivat S., Satranarakun P., Traub R.J., Schaper R. Experimental infection with Ancylostoma ceylanicum in dogs and efficacy of a spot on combination containing imidacloprid 10% and moxidectin 2.5% (Advocate/Advantage Multi, Bayer Animal Health). Parasitol. Res. 2010, 106:1499-1502.
65. Taweethavonsawat P., Chungpivat S., Watanapongchati S., Traub R.J., Schaper R. Efficacy of a spot on combination containing imidacloprid 10% and moxidectin 1% (Advocate((R))/Advantage((R)) Multi, Bayer Animal Health) against Ancylostoma ceylanicum in cats. Vet. Parasitol. 2012, 190:289-293.
66. Taweethavonsawat P., Chungpivat S., Watanapongchati S., Traub R.J., Schaper R. Comparative efficacy of a spot-on formulation containing emodepside and praziquantel (Profender®, Bayer) and praziquantel and pyrantel oral tablets (Drontal® for Cats) against experimental Ancylostoma ceylanicum infections in cats. Vet. Parasitol. 2013, 191:172-176.
67. Traub R.J., Hobbs R.P., Adams P.J., Behnke J.M., Harris P.D., Thompson R.C. A case of mistaken identity- reappraisal of the species of canid and felid hookworms (Ancylostoma) present in Australia and India. Parasitology 2007, 134:113-119.
68. Traub R.J., Inpankaew T., Sutthikornchai C., Sukthana Y., Thompson R.C. PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in Bangkok. Vet. Parasitol. 2008, 155:67-73.
69. Traub R.J., Robertson I.D., Irwin P., Mencke N., Thompson R.C. Application of a species-specific PCR-RFLP to identify Ancylostoma eggs directly from canine faeces. Vet. Parasitol. 2004, 123:245-255.
70. Traub R.J., Robertson I.D., Irwin P.J., Mencke N., Thompson R.C. Canine gastrointestinal parasitic zoonoses in India. Trends Parasitol. 2005, 21:42-48.
71. Velasquez C.C., Cabrera B.C. Ancylostoma ceylanicum (Looss, 1911) in a Filipino woman. J. Parasitol. 1968, 54:430-431.
72. Visen P.K., Katiyar J.C., Sen A.B. Studies on infectivity, longevity and fecundity of Ancylostoma ceylanicum in golden hamsters. J. Helminthol. 1984, 58:159-163.
73. Walker, A., 1952. Clinical Problems of War - Ankylostomiasis, Australia in the War of 1939-1945. Series 5 - Medical Australian War Memorial, Australian Government, Australia.
74. Wang C.H., Lee S.C., Huang S.S., Chang L.C. Hookworm infection in a healthy adult that manifested as severe eosinophilia and diarrhea. J. Microbiol. Immunol. Infect. 2011, 44:484-487.
75. Whipple G. Uncinarias is in Panama. Am. J. Med. Sci. 1909, 138:40-48.
76. Wijers D.J., Smit A.M. Early symptoms after experimental infection of man with Ancylostoma braziliense var. ceylanicum. Trop. Geog. Med. 1966, 18:48-52.
77. World Health Organization, 2002. Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee, WHO Technical Report Series no. 912, pp. 1-57.
78. World Health Organization, 2005. WHO Expert Consultation on Rabies, Technical Report Series 931, Geneva.
79. Yoshida Y. Comparative studies on Ancylostoma braziliense and Ancylostoma ceylanicum I. The adult stage. J. Parasitol. 1971, 57:983-989.
80. Yoshida Y., Okamoto K. On the hookworms in stray dogs in Kagoshima Prefecture, southern part of Japan, with special reference to Ancylostoma ceylanicum. Jpn. J. Parasitol. 1972, 21:328-332.
81. Yoshida Y., Kondo K., Kurimoto H., Fukutome S., Shirasaka S. Comparative studies on Ancylostoma braziliense and Ancylostoma ceylanicum. 3. Life history in the definitive host. J. Parasitol. 1974, 60:636-641.
82. Yoshida Y., Okamoto K., Chiu J.K. Ancylostoma ceylanicum infection in dogs, cats, and man in Taiwan. Am. J. Trop. Med. Hyg. 1968, 17:378-381.
83. Yoshida Y., Okamoto K., Chiu J.K. Experimental infection of man with Ancylostoma ceylanicum Looss, 1911. Chin. J. Microbiol. 1971, 4:157-167.
84. Yoshida Y., Okamoto K., Matsuo K., Kwo E.H., 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, 4:498-503.
85. Ziegelbauer K., Speich B., Mausezahl D., Bos R., Keiser J., Utzinger J. Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med. 2012, 9:e1001162.