Hookworm infection

Nature Reviews Disease Primers

Volumn 2, Issue , 2016, Pages

  Loukas, Alex ^a   Hotez, Peter J ^b,c,d   Diemert, David ^e,f   Yazdanbakhsh, Maria ^g   McCarthy, James S ^h,i   Correa Oliveira, Rodrigo ^j   Croese, John ^a,k   Bethony, Jeffrey M ^e  

^a JAMES COOK UNIVERSITY   (Australia)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c Sabin Vaccine Institute   (United States)

^d TEXAS CHILDREN S HOSPITAL   (United States)

^e GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^f Sabin Vaccine Institute   (United States)

^g LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^h QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

ⁱ UNIVERSITY OF QUEENSLAND   (Australia)

^j INSTITUTO OSWALDO CRUZ   (Brazil)

^k THE PRINCE CHARLES HOSPITAL   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BENZIMIDAZOLE DERIVATIVE; ALBENDAZOLE; ANTHELMINTIC AGENT; BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 11A; BLOOD CLOTTING FACTOR 7A; MEBENDAZOLE;

ANIMAL MODEL; ARTICLE; BLEEDING; COMORBIDITY; ENVIRONMENTAL SANITATION; HIGH RISK POPULATION; HOOKWORM INFECTION; HUMAN; HYGIENE; IMMUNE RESPONSE; IMMUNOBIOLOGY; IMMUNOPATHOLOGY; INFECTION PREVENTION; INFLAMMATION; MORBIDITY; MORTALITY; NONHUMAN; POVERTY; PREVALENCE; PRIORITY JOURNAL; PRODUCTIVITY; QUALITY OF LIFE; SPECIES INVASION; WATER QUALITY; ZOONOSIS; ANEMIA; ANIMAL; COMPLICATION; FECES; HOOKWORM; IMMUNOLOGY; LARVA MIGRANS; NECATOR AMERICANUS; PARASITOLOGY; PATHOGENICITY; PATHOPHYSIOLOGY; RISK FACTOR; SMALL INTESTINE; SOIL;

ALBENDAZOLE; ANCYLOSTOMATOIDEA; ANEMIA; ANIMALS; ANTHELMINTICS; FACTOR VIIA; FACTOR XA; FACTOR XIA; FECES; HEMORRHAGE; HOOKWORM INFECTIONS; HUMANS; INTESTINE, SMALL; LARVA MIGRANS; MEBENDAZOLE; NECATOR AMERICANUS; PREVALENCE; RISK FACTORS; SOIL;

EID: 85003698454     PISSN: None     EISSN: 2056676X     Source Type: Journal    
DOI: 10.1038/nrdp.2016.88     Document Type: Article

References (206)

1. Pullan, R. L., Smith, J. L., Jasrasaria, R., Brooker, S. J. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit. Vectors 7, 37 (2014).
2. Bartsch, S. M., et al. The global economic and health burden of human hookworm infection. PLoS Negl. Trop. Dis. 10, e0004922 (2016).
3. Brown, E. R. Public health in imperialism: early Rockefeller programs at home and abroad. Am. J. Public Health 66, 897-903 (1976).
4. International Health Division of the Rockefeller Foundation. Unhooking the hookworm. YouTube https://www. youtube. com/watchv=OD-sDlSDrKk (1920).
5. Bartsch, S. M., et al. Modeling the economic and epidemiologic impact of hookworm vaccine and mass drug administration (MDA) in Brazil, a high transmission setting. Vaccine 34, 2197-2206 (2016).
6. De Clercq, D., et al. Failure of mebendazole in treatment of human hookworm infections in the southern region of Mali. Am. J. Trop. Med. Hyg. 57, 25-30 (1997).
7. Soukhathammavong, P. A., et al. Low efficacy of single-dose albendazole and mebendazole against hookworm and effect on concomitant helminth infection in Lao PDR. PLoS Negl. Trop. Dis. 6, e1417 (2012).
8. Albonico, M., et al. Rate of reinfection with intestinal nematodes after treatment of children with mebendazole or albendazole in a highly endemic area. Trans. R. Soc. Trop. Med. Hyg. 89, 538-541 (1995).
9. Croese, J., et al. Experimental hookworm infection and gluten microchallenge promote tolerance in celiac disease. J. Allergy Clin. Immunol. 135, 508-516 (2015).
10. Croese, J., et al. A proof of concept study establishing Necator americanus in Crohn's patients and reservoir donors. Gut 55, 136-137 (2006).
11. Feary, J., et al. Safety of hookworm infection in individuals with measurable airway responsiveness: a randomized placebo-controlled feasibility study. Clin. Exp. Allergy 39, 1060-1068 (2009).
12. Summers, R. W., et al. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128, 825-832 (2005).
13. Inpankaew, T., et al. High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012. Emerg. Infect. Dis. 20, 976-982 (2014).
14. Traub, R. J. Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis. Int. J. Parasitol. 43, 1009-1015 (2013).
15. Hotez, P. Hookworm and poverty. Ann. NY Acad. Sci. 1136, 38-44 (2008).
16. Haswell-Elkins, M. R., Elkins, D. B., Manjula, K., Michael, E., Anderson, R. M. An investigation of hookworm infection and reinfection following mass anthelmintic treatment in the south Indian fishing community of Vairavankuppam. Parasitology 96, 565-577 (1988).
17. Montresor, A., Compton, D. W. T., Hall, A., Bundy, D. A. P., Savioli, L. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level (WHO, 1998).
18. Roche, M., Layrisse, M. The nature and causes of "hookworm anemia". Am. J. Trop. Med. Hyg. 15, 1029-1102 (1966).
19. Albonico, M., et al. Epidemiological evidence for a differential effect of hookworm species. Ancylostoma duodenale or Necator americanus, on iron status of children. Int. J. Epidemiol. 27, 530-537 (1998).
20. Brooker, S., et al. Epidemiology of plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, prospects for combining control. Am. J. Trop. Med. Hyg. 77, 88-98 (2007).
21. GBD 2013 Mortality and Causes of Death Collaborators. Global, regional, national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 385, 117-171 (2015).
22. Hotez, P. J., Bottazzi, M. E., Strych, U. New vaccines for the world's poorest people. Annu. Rev. Med. 67, 405-417 (2016).
23. Kassebaum, N. J., GBD 2013 Anemia Collaborators. The global burden of anemia. Hematol. Oncol. Clin. North Am. 30, 247-308 (2016).
24. Anderson, R. M., Truscott, J. E., Pullan, R. L., Brooker, S. J., Hollingsworth, T. D. How effective is school-based deworming for the community-wide control of soil-transmitted helminths PLoS Negl. Trop. Dis. 7, e2027 (2013).
25. Bethony, J., et al. Emerging patterns of hookworm infection: influence of aging on the intensity of Necator infection in Hainan Province, People's Republic of China. Clin. Infect. Dis. 35, 1336-1344 (2002).
26. Hotez, P. J., et al. Hookworm infection. N. Engl. J. Med. 351, 799-807 (2004).
27. Smith, J. L., Brooker, S. Impact of hookworm infection and deworming on anaemia in non-pregnant populations: a systematic review. Trop. Med. Int. Health 15, 776-795 (2010).
28. Crompton, D. W. The public health importance of hookworm disease. Parasitology 121, S39-S50 (2000).
29. Blackwell, A. D., et al. Helminth infection, fecundity, age of first pregnancy in women. Science 350, 970-972 (2015).
30. Dickson, R., Awasthi, S., Williamson, P., Demellweek, C., Garner, P. Effects of treatment for intestinal helminth infection on growth and cognitive performance in children: systematic review of randomised trials. BMJ 320, 1697-1701 (2000).
31. Sakti, H., et al. Evidence for an association between hookworm infection and cognitive function in Indonesian school children. Trop. Med. Int. Health 4, 322-334 (1999).
32. Jardim-Botelho, A., et al. Hookworm, Ascaris lumbricoides infection and polyparasitism associated with poor cognitive performance in Brazilian schoolchildren. Trop. Med. Int. Health 13, 994-1004 (2008).
33. Brooker, S., Hotez, P. J., Bundy, D. A. Hookworm-related anaemia among pregnant women: a systematic review. PLoS Negl. Trop. Dis. 2, e291 (2008).
34. Christian, P., Khatry, S. K., West, K. P. Jr. Antenatal anthelmintic treatment, birthweight, infant survival in rural Nepal. Lancet 364, 981-983 (2004).
35. Bundy, D. A., Chan, M. S., Savioli, L. Hookworm infection in pregnancy. Trans. R. Soc. Trop. Med. Hyg. 89, 521-522 (1995).
36. Menzies, S. K., et al. Risk factors for soil-transmitted helminth infections during the first 3 years of life in the tropics; findings from a birth cohort. PLoS Negl. Trop. Dis. 8, e2718 (2014).
37. World Health Organization. Report of the WHO Informal Consultation on Hookworm Infection and Anaemia in Girls and Women (WHO, 1994).
38. Brand, A., Hawdon, J. M. Phosphoinositide-3-OH-kinase inhibitor LY294002 prevents activation of Ancylostoma caninum and Ancylostoma ceylanicum third-stage infective larvae. Int. J. Parasitol. 34, 909-914 (2004).
39. Yoshida, Y., Matsuo, K., Kondo, K., Arizono, N., Ogino, K. Scanning electron microscopy of hookworms. 1. Adults and infective-stage larvae of Necator americanus (Stiles, 1902). Southeast Asian J. Trop. Med. Public Health 5, 510-514 (1974).
40. Brown, A., Girod, N., Billett, E. E., Pritchard, D. I. Necator americanus (human hookworm) aspartyl proteinases and digestion of skin macromolecules during skin penetration. Am. J. Trop. Med. Hyg. 60, 840-847 (1999).
41. Hotez, P. J., et al. Hyaluronidase from infective Ancylostoma hookworm larvae and its possible function as a virulence factor in tissue invasion and in cutaneous larva migrans. Infect. Immun. 60, 1018-1023 (1992).
42. Hawdon, J. M., Jones, B. F., Hoffman, D. R., Hotez, P. J. Cloning and characterization of Ancylostoma-secreted protein. A novel protein associated with the transition to parasitism by infective hookworm larvae. J. Biol. Chem. 271, 6672-6678 (1996).
43. Mulvenna, J., et al. Proteomics analysis of the excretory/secretory component of the blood-feeding stage of the hookworm, Ancylostoma caninum. Mol. Cell Proteomics 8, 109-121 (2009).
44. Tang, Y. T., et al. Genome of the human hookworm Necator americanus. Nat. Genet. 46, 261-269 (2014).
45. Diemert, D. J., et al. Generalized urticaria induced by the Na-ASP-2 hookworm vaccine: implications for the development of vaccines against helminths. J. Allergy Clin. Immunol. 130, 169-176. e6 (2012).
46. Ranjit, N., et al. Proteolytic degradation of hemoglobin in the intestine of the human hookworm Necator americanus. J. Infect. Dis. 199, 904-912 (2009).
47. Zhan, B., et al. Biochemical characterization and vaccine potential of a heme-binding glutathione transferase from the adult hookworm Ancylostoma caninum. Infect. Immun. 73, 6903-6911 (2005).
48. Stassens, P., et al. Anticoagulant repertoire of the hookworm Ancylostoma caninum. Proc. Natl Acad. Sci. USA 93, 2149-2154 (1996).
49. Layrisse, M., Linares, J., Roche, M. Excess hemolysis in subjects with severe iron deficiency anemia associated and nonassociated with hookworm infection. Blood 25, 73-91 (1965).
50. Hoeppli, R. Parasites and Parasitic Infections in Early Science and Medicine (Univ. of Malaya Press, 1959).
51. Basta, S. S., Soekirman, Karyadi, D., Scrimshaw, N. S. Iron deficiency anemia and the productivity of adult males in Indonesia. Am. J. Clin. Nutr. 32, 916-925 (1979).
52. Mugisha, J. O., Baisley, K., Asiki, G., Seeley, J., Kuper, H. Prevalence, types, risk factors and clinical correlates of anaemia in older people in a rural Ugandan population. PLoS ONE 8, e78394 (2013).
53. Olsen, A., Magnussen, P., Ouma, J. H., Andreassen, J., Friis, H. The contribution of hookworm and other parasitic infections to haemoglobin and iron status among children and adults in western Kenya. Trans. R. Soc. Trop. Med. Hyg. 92, 643-649 (1998).
54. Stoltzfus, R. J., Dreyfuss, M. L., Chwaya, H. M., Albonico, M. Hookworm control as a strategy to prevent iron deficiency. Nutr. Rev. 55, 223-232 (1997).
55. Hotez, P. J. China's hookworms. China Q. 172, 1029-1041 (2002).
56. Blount, D., et al. Immunologic profiles of persons recruited for a randomized, placebo-controlled clinical trial of hookworm infection. Am. J. Trop. Med. Hyg. 81, 911-916 (2009).
57. Maxwell, C., et al. The clinical and immunologic responses of normal human volunteers to low dose hookworm (Necator americanus) infection. Am. J. Trop. Med. Hyg. 37, 126-134 (1987).
58. Gaze, S., et al. Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLoS Pathog. 8, e1002520 (2012).
59. Daveson, A. J., et al. Effect of hookworm infection on wheat challenge in celiac disease-a randomised double-blinded placebo controlled trial. PLoS ONE 6, e17366 (2011).
60. Bowman, D. D., Montgomery, S. P., Zajac, A. M., Eberhard, M. L., Kazacos, K. R. Hookworms of dogs and cats as agents of cutaneous larva migrans. Trends Parasitol. 26, 162-167 (2010).
61. Guill, M. A., Odom, R. B. Larva migrans complicated by Loeffler's syndrome. Arch. Dermatol. 114, 1525-1526 (1978).
62. Prociv, P., Croese, J. Human eosinophilic enteritis caused by dog hookworm Ancylostoma caninum. Lancet 335, 1299-1302 (1990).
63. Croese, J., Loukas, A., Opdebeeck, J., Prociv, P. Occult enteric infection by Ancylostoma caninum: a previously unrecognized zoonosis. Gastroenterology 106, 3-12 (1994).
64. Khoshoo, V., et al. Dog hookworm: a cause of eosinophilic enterocolitis in humans. J. Pediatr. Gastroenterol. Nutr. 19, 448-452 (1994).
65. Bahgat, M. A., El Gindy, A. E., Mahmoud, L. A., Hegab, M. H., Shahin, A. M. Evaluation of the role of Ancylostoma caninum in humans as a cause of acute and recurrent abdominal pain. J. Egypt Soc. Parasitol. 29, 873-882 (1999).
66. Prociv, P., Croese, J. Human enteric infection with Ancylostoma caninum: hookworms reappraised in the light of a "new" zoonosis. Acta Trop. 62, 23-44 (1996).
67. Behnke, J. M., Paul, V., Rajasekariah, G. R. The growth and migration of Necator americanus following infection of neonatal hamsters. Trans. R. Soc. Trop. Med. Hyg. 80, 146-149 (1986).
68. Jian, X., et al. Necator americanus: maintenance through one hundred generations in golden hamsters (Mesocricetus auratus). I. Host sex-associated differences in hookworm burden and fecundity. Exp. Parasitol. 104, 62-66 (2003).
69. Camberis, M., Le Gros, G., Urban, J. Jr. Animal model of Nippostrongylus brasiliensis and Heligmosomoides polygyrus. Curr. Protoc. Immunol. 55, 19. 12. 1-19. 12. 27 (2003).
70. Nair, M. G., Herbert, D. R. Immune polarization by hookworms: taking cues from T helper type 2, type 2 innate lymphoid cells and alternatively activated macrophages. Immunology 148, 115-124 (2016).
71. Bungiro, R. D., et al. Mucosal antibody responses in experimental hookworm infection. Parasite Immunol. 30, 293-303 (2008).
72. Wells, C., Behnke, J. M. Acquired resistance to the human hookworm Necator americanus in mice. Parasite Immunol. 10, 493-505 (1988).
73. Reynolds, L. A., Filbey, K. J., Maizels, R. M. Immunity to the model intestinal helminth parasite Heligmosomoides polygyrus. Semin. Immunopathol. 34, 829-846 (2012).
74. Held, M. R., Bungiro, R. D., Harrison, L. M., Hamza, I., Cappello, M. Dietary iron content mediates hookworm pathogenesis in vivo. Infect. Immun. 74, 289-295 (2006).
75. Alkazmi, L. M., Behnke, J. M. The mucosal response of hamsters to a low-intensity superimposed secondary infection with the hookworm Ancylostoma ceylanicum. J. Helminthol. 85, 56-65 (2011).
76. Xiao, S., et al. The evaluation of recombinant hookworm antigens as vaccines in hamsters (Mesocricetus auratus) challenged with human hookworm. Necator americanus. Exp. Parasitol. 118, 32-40 (2008).
77. Miller, T. A. Transfer of immunity to Ancylostoma caninum infection in pups by serum and lymphoid cells. Immunology 12, 231-241 (1967).
78. Geiger, S. M., Fujiwara, R. T., Santiago, H., Correa-Oliveira, R., Bethony, J. M. Early stage-specific immune responses in primary experimental human hookworm infection. Microbes Infect. 10, 1524-1535 (2008).
79. Fujiwara, R. T., Geiger, S. M., Bethony, J., Mendez, S. Comparative immunology of human and animal models of hookworm infection. Parasite Immunol. 28, 285-293 (2006).
80. Griffiths, G. D., et al. Development of a model of hookworm infection exhibiting salient characteristics of human infection. Am. J. Trop. Med. Hyg. 78, 936-945 (2008).
81. Navarro, S., Ferreira, I., Loukas, A. The hookworm pharmacopoeia for inflammatory diseases. Int. J. Parasitol. 43, 225-231 (2013).
82. Girod, N., Brown, A., Pritchard, D. I., Billett, E. E. Successful vaccination of BALB/c mice against human hookworm (Necator americanus): the immunological phenotype of the protective response. Int. J. Parasitol. 33, 71-80 (2003).
83. Obata-Ninomiya, K., et al. The skin is an important bulwark of acquired immunity against intestinal helminths. J. Exp. Med. 210, 2583-2595 (2013).
84. Scrivener, S., et al. Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: a nested case-control study. Lancet 358, 1493-1499 (2001).
85. Chen, F., et al. Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion. Nat. Immunol. 15, 938-946 (2014).
86. Gerbe, F., et al. Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites. Nature 529, 226-230 (2016).
87. Ball, P. A., Bartlett, A. Serological reactions to infection with Necator americanus. Trans. R. Soc. Trop. Med. Hyg. 63, 362-369 (1969).
88. Quinnell, R. J., Bethony, J., Pritchard, D. I. The immunoepidemiology of human hookworm infection. Parasite Immunol. 26, 443-454 (2004).
89. Quinnell, R. J., Pritchard, D. I., Raiko, A., Brown, A. P., Shaw, M. A. Immune responses in human necatoriasis: association between interleukin-5 responses and resistance to reinfection. J. Infect. Dis. 190, 430-438 (2004).
90. Cooper, P. J., et al. Geohelminth infections: a review of the role of IgE and assessment of potential risks of anti-IgE treatment. Allergy 63, 409-417 (2008).
91. Grove, D. I., Burston, T. O., Forbes, I. J. Fall in IgE levels after treatment for hookworm. Clin. Exp. Immunol. 18, 565-569 (1974).
92. Grove, D. I., Forbes, I. J. Increased resistance to helminth infestation in an atopic population. Med. J. Aust. 1, 336-338 (1975).
93. Falcone, F. H., et al. Antigen-driven basophil activation is indicative of early Necator americanus infection in IgE-seronegative patients. J. Allergy Clin. Immunol. 124, 1343-1350. e7 (2009).
94. Maizels, R. M., Yazdanbakhsh, M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3, 733-744 (2003).
95. Loukas, A., Opdebeeck, J., Croese, J., Prociv, P. Immunoglobulin G subclass antibodies against excretory/secretory antigens of Ancylostoma caninum in human enteric infections. Am. J. Trop. Med. Hyg. 54, 672-676 (1996).
96. Palmer, D. R., Bradley, M., Bundy, D. A. IgG4 responses to antigens of adult Necator americanus: potential for use in large-scale epidemiological studies. Bull. World Health Organ. 74, 381-386 (1996).
97. McSorley, H. J., Loukas, A. The immunology of human hookworm infections. Parasite Immunol. 32, 549-559 (2010).
98. Allen, J. E., Sutherland, T. E. Host protective roles of type 2 immunity: parasite killing and tissue repair, flip sides of the same coin. Semin. Immunol. 26, 329-340 (2014).
99. Wammes, L. J., Mpairwe, H., Elliott, A. M., Yazdanbakhsh, M. Helminth therapy or elimination: epidemiological, immunological, clinical considerations. Lancet Infect. Dis. 14, 1150-1162 (2014).
100. Ricci, N. D., et al. Induction of CD4+CD25+FOXP3+ regulatory T cells during human hookworm infection modulates antigen-mediated lymphocyte proliferation. PLoS Negl. Trop. Dis. 5, e1383 (2011).
101. Brenchley, J. M., Douek, D. C. Microbial translocation across the GI tract. Annu. Rev. Immunol. 30, 149-173 (2012).
102. George, P. J., et al. Evidence of microbial translocation associated with perturbations in T cell and antigen-presenting cell homeostasis in hookworm infections. PLoS Negl. Trop. Dis. 6, e1830 (2012).
103. Verweij, J. J. Application of PCR-based methods for diagnosis of intestinal parasitic infections in the clinical laboratory. Parasitology 141, 1863-1872 (2014).
104. Easton, A. V., et al. Multi-parallel qPCR provides increased sensitivity and diagnostic breadth for gastrointestinal parasites of humans: field-based inferences on the impact of mass deworming. Parasit. Vectors 9, 38 (2016).
105. Cimino, R. O., et al. Identification of human intestinal parasites affecting an asymptomatic peri-urban Argentinian population using multi-parallel quantitative real-time polymerase chain reaction. Parasit. Vectors 8, 380 (2015).
106. Coffeng, L. E., Bakker, R., Montresor, A., de Vlas, S. J. Feasibility of controlling hookworm infection through preventive chemotherapy: a simulation study using the individual-based WORMSIM modelling framework. Parasit. Vectors 8, 541 (2015).
107. Strunz, E. C., et al. Water, sanitation, hygiene, soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 11, e1001620 (2014).
108. Cairncross, S., et al. Water, sanitation and hygiene for the prevention of diarrhoea. Int. J. Epidemiol. 39 (Suppl. 1), i193-i205 (2010).
109. Clasen, T. F., et al. Interventions to improve disposal of human excreta for preventing diarrhoea. Cochrane Database Syst. Rev. 6, CD007180 (2010).
110. Hunter, P. R., Ramirez Toro, G. I., Minnigh, H. A. Impact on diarrhoeal illness of a community educational intervention to improve drinking water quality in rural communities in Puerto Rico. BMC Public Health 10, 219 (2010).
111. Bieri, F. A., et al. Health-education package to prevent worm infections in Chinese schoolchildren. N. Engl. J. Med. 368, 1603-1612 (2013).
112. Bird, C., Ame, S., Albonico, M., Bickle, Q. Do shoes reduce hookworm infection in school-aged children on Pemba Island, Zanzibar A pragmatic trial. Trans. R. Soc. Trop. Med. Hyg. 108, 297-304 (2014).
113. Ziegelbauer, K., et al. Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med. 9, e1001162 (2012).
114. Freeman, M. C., Clasen, T. Assessing the impact of a school-based safe water intervention on household adoption of point-of-use water treatment practices in southern India. Am. J. Trop. Med. Hyg. 84, 370-378 (2011).
115. Hong, S. T., et al. A successful experience of soil-transmitted helminth control in the Republic of Korea. Korean J. Parasitol. 44, 177-185 (2006).
116. Kobayashi, A., Hara, T., Kajima, J. Historical aspects for the control of soil-transmitted helminthiases. Parasitol. Int. 55, S289-S291 (2006).
117. Hawdon, J. M. Controlling soil-transmitted helminths: time to think inside the box J. Parasitol. 100, 166-188 (2014).
118. Keiser, J., Utzinger, J. Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA 299, 1937-1948 (2008).
119. Vercruysse, J., et al. Assessment of the anthelmintic efficacy of albendazole in school children in seven countries where soil-transmitted helminths are endemic. PLoS Negl. Trop. Dis. 5, e948 (2011).
120. Steinmann, P., et al. Efficacy of single-dose and triple-dose albendazole and mebendazole against soil-transmitted helminths and Taenia spp. : a randomized controlled trial. PLoS ONE 6, e25003 (2011).
121. Belew, S., et al. Assessment of efficacy and quality of two albendazole brands commonly used against soil-transmitted helminth infections in school children in Jimma Town, Ethiopia. PLoS Negl. Trop. Dis. 9, e0004057 (2015).
122. Albonico, M., et al. Efficacy of mebendazole and levamisole alone or in combination against intestinal nematode infections after repeated targeted mebendazole treatment in Zanzibar. Bull. World Health Organ. 81, 343-352 (2003).
123. Demeler, J., et al. Phylogenetic characterization of beta-tubulins and development of pyrosequencing assays for benzimidazole resistance in cattle nematodes. PLoS ONE 8, e70212 (2013).
124. Diawara, A., et al. Association between response to albendazole treatment and-tubulin genotype frequencies in soil-transmitted helminths. PLoS Negl. Trop. Dis. 7, e2247 (2013).
125. Dayan, A. D. Albendazole, mebendazole and praziquantel. Review of non-clinical toxicity and pharmacokinetics. Acta Trop. 86, 141-159 (2003).
126. Ndyomugyenyi, R., Kabatereine, N., Olsen, A., Magnussen, P. Efficacy of ivermectin and albendazole alone and in combination for treatment of soil-transmitted helminths in pregnancy and adverse events: a randomized open label controlled intervention trial in Masindi district, western Uganda. Am. J. Trop. Med. Hyg. 79, 856-863 (2008).
127. Montresor, A., Awasthi, S., Crompton, D. W. Use of benzimidazoles in children younger than 24 months for the treatment of soil-transmitted helminthiasis. Acta Trop. 86, 223-232 (2003).
128. World Health Organization. Report of the WHO Informal Consultation on the Use of Praziquantel During Pregnancy/Lactation and Albendazole/Mebendazole in Children Under 24 Months (WHO, 2002).
129. Kohler, P. The biochemical basis of anthelmintic action and resistance. Int. J. Parasitol. 31, 336-345 (2001).
130. Steinmann, P., et al. Tribendimidine and albendazole for treating soil-transmitted helminths. Strongyloides stercoralis and Taenia spp. : open-label randomized trial. PLoS Negl. Trop. Dis. 2, e322 (2008).
131. Xiao, S. H., Utzinger, J., Tanner, M., Keiser, J., Xue, J. Advances with the Chinese anthelminthic drug tribendimidine in clinical trials and laboratory investigations. Acta Trop. 126, 115-126 (2013).
132. Hu, Y., Platzer, E. G., Bellier, A., Aroian, R. V. Discovery of a highly synergistic anthelmintic combination that shows mutual hypersusceptibility. Proc. Natl Acad. Sci. USA 107, 5955-5960 (2010).
133. Hu, Y., et al. Mechanistic and single-dose in vivo therapeutic studies of Cry5B anthelmintic action against hookworms. PLoS Negl. Trop. Dis. 6, e1900 (2012).
134. Keiser, J., et al. Activity of oxantel pamoate monotherapy and combination chemotherapy against Trichuris muris and hookworms: revival of an old drug. PLoS Negl. Trop. Dis. 7, e2119 (2013).
135. Speich, B., et al. Efficacy and reinfection with soil-transmitted helminths 18-weeks post-treatment with albendazole-ivermectin, albendazole-mebendazole, albendazole-oxantel pamoate and mebendazole. Parasit. Vectors 9, 123 (2016).
136. Rajagopal, S., Hotez, P. J., Bundy, D. A. Micronutrient supplementation and deworming in children with geohelminth infections. PLoS Negl. Trop. Dis. 8, e2920 (2014).
137. Torlesse, H., Hodges, M. Albendazole therapy and reduced decline in haemoglobin concentration during pregnancy (Sierra Leone). Trans. R. Soc. Trop. Med. Hyg. 95, 195-201 (2001).
138. Montresor, A., et al. Is the exclusion of children under 24 months from anthelmintic treatment justifiable Trans. R. Soc. Trop. Med. Hyg. 96, 197-199 (2002).
139. Truscott, J. E., Turner, H. C., Anderson, R. M. What impact will the achievement of the current World Health Organisation targets for anthelmintic treatment coverage in children have on the intensity of soil transmitted helminth infections Parasit. Vectors 8, 551 (2015).
140. Bundy, D. A., Michael, E., Guyatt, H. in The Biology of Nematodes (ed. Lee, D. L. ) 599-617 (Taylor and Francis, 2002).
141. Savioli, L., et al. Schistosomiasis and soil-transmitted helminth infections: forging control efforts. Trans. R. Soc. Trop. Med. Hyg. 96, 577-579 (2002).
142. Awasthi, S., Pande, V. K., Fletcher, R. H. Effectiveness and cost-effectiveness of albendazole in improving nutritional status of pre-school children in urban slums. Indian Pediatr. 37, 19-29 (2000).
143. Taylor-Robinson, D., Jones, A., Garner, P. Does deworming improve growth and school performance in children PLoS Negl. Trop. Dis. 3, e358 (2009).
144. Yap, P., et al. Rapid re-infection with soil-transmitted helminths after triple-dose albendazole treatment of school-aged children in Yunnan, People's Republic of China. Am. J. Trop. Med. Hyg. 89, 23-31 (2013).
145. Supali, T., et al. Impact of six rounds of mass drug administration on Brugian filariasis and soil-transmitted helminth infections in eastern Indonesia. PLoS Negl. Trop. Dis. 7, e2586 (2013).
146. Geerts, S., Coles, G. C., Gryseels, B. Anthelmintic resistance in human helminths: learning from the problems with worm control in livestock. Parasitol. Today 13, 149-151; discussion 156 (1997).
147. Humphries, D., et al. Epidemiology of hookworm infection in Kintampo North Municipality, Ghana: patterns of malaria coinfection, anemia, albendazole treatment failure. Am. J. Trop. Med. Hyg. 84, 792-800 (2011).
148. Stothard, J. R., Rollinson, D., Imison, E., Khamis, I. S. A spot-check of the efficacies of albendazole or levamisole, against soil-transmitted helminthiases in young Ungujan children, reveals low frequencies of cure. Ann. Trop. Med. Parasitol. 103, 357-360 (2009).
149. Taylor-Robinson, D. C., Maayan, N., Soares-Weiser, K., Donegan, S., Garner, P. Deworming drugs for soil-transmitted intestinal worms in children: effects on nutritional indicators, haemoglobin, school performance. Cochrane Database Syst. Rev. 7, CD000371 (2015).
150. Adegnika, A. A., et al. Randomized, controlled, assessor-blind clinical trial to assess the efficacy of single-versus repeated-dose albendazole to treat Ascaris lumbricoides. Trichuris trichiura, hookworm infection. Antimicrob. Agents Chemother. 58, 2535-2540 (2014).
151. Lenk, E. J., Redekop, W. K., Luyendijk, M., Rijnsburger, A. J., Severens, J. L. Productivity loss related to neglected tropical diseases eligible for preventive chemotherapy: a systematic literature review. PLoS Negl. Trop. Dis. 10, e0004397 (2016).
152. Hotez, P., Whitham, M. Helminth infections: a new global women's health agenda. Obstet. Gynecol. 123, 155-160 (2014).
153. Stephenson, L. S., Latham, M. C., Adams, E. J., Kinoti, S. N., Pertet, A. Physical fitness, growth and appetite of Kenyan school boys with hookworm. Trichuris trichiura and Ascaris lumbricoides infections are improved four months after a single dose of albendazole. J. Nutr. 123, 1036-1046 (1993).
154. Smillie, W. G., Augustine, D. L. Hookworm infestation: the effects of varying intensities on the physical condition of school children. Am. J. Dis. Child 31, 151-168 (1926).
155. Smillie, W. G., Spencer, C. R. Mental retardation in school children infested with hookworms. J. Educ. Pyschol. 17, 314-321 (1926).
156. Hurlimann, E., et al. Health-related quality of life among school children with parasitic infections: findings from a national cross-sectional survey in Cote d'Ivoire. PLoS Negl. Trop. Dis. 8, e3287 (2014).
157. Ziegelbauer, K., et al. Self-rated quality of life and school performance in relation to helminth infections: case study from Yunnan, People's Republic of China. Parasit. Vectors 3, 61 (2010).
158. Bleakley, H. Disease and development: evidence from hookworm eradication in the American South. Q. J. Econ. 122, 73-117 (2007).
159. Hotez, P. J., Ferris, M. T. The antipoverty vaccines. Vaccine 24, 5787-5799 (2006).
160. Gilgen, D. D., Mascie-Taylor, C. G., Rosetta, L. L. Intestinal helminth infections, anaemia and labour productivity of female tea pluckers in Bangladesh. Trop. Med. Int. Health 6, 449-457 (2001).
161. Selvaratnam, R. R., de Silva, L. D., Pathmeswaran, A., de Silva, N. R. Nutritional status and productivity of Sri Lankan tea pluckers. Ceylon Med. J. 48, 114-118 (2003).
162. Schuster, A., et al. Life quality impairment caused by hookworm-related cutaneous larva migrans in resource-poor communities in Manaus, Brazil. PLoS Negl. Trop. Dis. 5, e1355 (2011).
163. Brooker, S., et al. The co-distribution of Plasmodium falciparum and hookworm among African schoolchildren. Malar. J. 5, 99 (2006).
164. Raso, G., et al. An integrated approach for risk profiling and spatial prediction of Schistosoma mansoni-hookworm coinfection. Proc. Natl Acad. Sci. USA 103, 6934-6939 (2006).
165. Hotez, P. J., Molyneux, D. H. Tropical anemia: one of Africa's great killers and a rationale for linking malaria and neglected tropical disease control to achieve a common goal. PLoS Negl. Trop. Dis. 2, e270 (2008).
166. Hotez, P. J., Bethony, J. M., Oliveira, S. C., Brindley, P. J., Loukas, A. Multivalent anthelminthic vaccine to prevent hookworm and schistosomiasis. Expert Rev. Vaccines 7, 745-752 (2008).
167. World Health Organization. Soil-transmitted helminthiasis. Progress report on number of children treated with anthelminthic drugs: an update towards the 2010 global target. Wkly Epidemiol. Rec. 82, 237-252 (2008).
168. Turner, H. C., et al. An economic evaluation of expanding hookworm control strategies to target the whole community. Parasit. Vectors 8, 570 (2015).
169. Hotez, P. J., Strych, U., Lustigman, S., Bottazzi, M. E. Human anthelminthic vaccines: rationale and challenges. Vaccine 34, 3549-3555 (2016).
170. Hotez, P. J., et al. Advancing a vaccine to prevent hookworm disease and anemia. Vaccine 34, 3001-3005 (2016).
171. Hotez, P. J., Bethony, J. M., Diemert, D. J., Pearson, M., Loukas, A. Developing vaccines to combat hookworm infection and intestinal schistosomiasis. Nat. Rev. Microbiol. 8, 814-826 (2010).
172. Loukas, A., Bethony, J., Brooker, S., Hotez, P. Hookworm vaccines: past, present, future. Lancet Infect. Dis. 6, 733-741 (2006).
173. Yazdanbakhsh, M., Kremsner, P. G., van Ree, R. Allergy, parasites, the hygiene hypothesis. Science 296, 490-494 (2002).
174. Rook, G. A., Brunet, L. R. Old friends for breakfast. Clin. Exp. Allergy 35, 841-842 (2005).
175. Hamid, F., et al. Risk factors associated with the development of atopic sensitization in Indonesia. PLoS ONE 8, e67064 (2013).
176. Wiria, A. E., et al. Infection with soil-transmitted helminths is associated with increased insulin sensitivity. PLoS ONE 10, e0127746 (2015).
177. Prideaux, L., Kamm, M. A., De Cruz, P. P., Chan, F. K., Ng, S. C. Inflammatory bowel disease in Asia: a systematic review. J. Gastroenterol. Hepatol. 27, 1266-1280 (2012).
178. Jackson, J. A., Friberg, I. M., Little, S., Bradley, J. E. Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies Immunology 126, 18-27 (2009).
179. Briggs, N., Weatherhead, J., Sastry, K. J., Hotez, P. J. The hygiene hypothesis and its inconvenient truths about helminth infections. PLoS Negl. Trop. Dis. 10, e0004944 (2016).
180. Helmby, H. Human helminth therapy to treat inflammatory disorders-where do we stand BMC Immunol. 16, 12 (2015).
181. Feary, J. R., et al. Experimental hookworm infection: a randomized placebo-controlled trial in asthma. Clin. Exp. Allergy 40, 299-306 (2010).
182. Giacomin, P., et al. Experimental hookworm infection and escalating gluten challenges are associated with increased microbial richness in celiac subjects. Sci. Rep. 5, 13797 (2015).
183. Zaiss, M. M., et al. The intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation. Immunity 43, 998-1010 (2015).
184. Cancado, G. G., et al. Hookworm products ameliorate dextran sodium sulfate-induced colitis in BALB/c mice. Inflamm. Bowel Dis. 17, 2275-2286 (2011).
185. Ferreira, I., et al. Hookworm excretory/secretory products induce interleukin-4 (IL-4)+ IL-10+ CD4+ T cell responses and suppress pathology in a mouse model of colitis. Infect. Immun. 81, 2104-2111 (2013).
186. Ruyssers, N. E., et al. Therapeutic potential of helminth soluble proteins in TNBS-induced colitis in mice. Inflamm. Bowel Dis. 15, 491-500 (2009).
187. Chhabra, S., et al. Kv1. 3 channel-blocking immunomodulatory peptides from parasitic worms: implications for autoimmune diseases. FASEB J. 28, 3952-3964 (2014).
188. Navarro, S., et al. Hookworm recombinant protein promotes regulatory T cell responses that suppress experimental asthma. Sci. Transl Med. 8, 362ra143 (2016).
189. Jiang, N., Moyle, M., Soule, H. R., Rote, W. E., Chopp, M. Neutrophil inhibitory factor is neuroprotective after focal ischemia in rats. Ann. Neurol. 38, 935-942 (1995).
190. Lees, K. R., Diener, H. C., Asplund, K., Krams, M., UK-279,276-301 Study Investigators. UK-279,276, a neutrophil inhibitory glycoprotein, in acute stroke: tolerability and pharmacokinetics. Stroke 34, 1704-1709 (2003).
191. Ledizet, M., Harrison, L. M., Koskia, R. A., Cappello, M. Discovery and pre-clinical development of antithrombotics from hematophagous invertebrates. Curr. Med. Chem. Cardiovasc. Hematol. Agents 3, 1-10 (2005).
192. Cox, F. E. History of human parasitology. Clin. Microbiol. Rev. 15, 595-612 (2002).
193. Maloy, K. J., Powrie, F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474, 298-306 (2011).
194. Lee, S. C., et al. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl. Trop. Dis. 8, e2880 (2014).
195. Cantacessi, C., et al. Impact of experimental hookworm infection on the human gut microbiota. J. Infect. Dis. 210, 1431-1434 (2014).
196. Cringoli, G., et al. Ancylostoma caninum: calibration and comparison of diagnostic accuracy of flotation in tube, McMaster and FLOTAC in faecal samples of dogs. Exp. Parasitol. 128, 32-37 (2011).
197. Barda, B. D., et al. Mini-FLOTAC, an innovative direct diagnostic technique for intestinal parasitic infections: experience from the field. PLoS Negl. Trop. Dis. 7, e2344 (2013).
198. Cringoli, G. FLOTAC, a novel apparatus for a multivalent faecal egg count technique. Parassitologia 48, 381-384 (2006).
199. Robertson, L. J., et al. Soil-transmitted helminth infections in school children from Cocle Province, Republic of Panama. Parasitology 99, 287-292 (1989).
200. Levecke, B., et al. A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato-Katz thick smear methods for soil-transmitted helminths. PLoS Negl. Trop. Dis. 5, e1201 (2011).
201. Pearson, M. S., Ranjit, N., Loukas, A. Blunting the knife: development of vaccines targeting digestive proteases of blood-feeding helminth parasites. Biol. Chem. 391, 901-911 (2010).
202. Karmakar, S., et al. Use of an Sm-p80-based therapeutic vaccine to kill established adult schistosome parasites in chronically infected baboons. J. Infect. Dis. 209, 1929-1940 (2014).
203. Loukas, A., et al. Vaccination with recombinant aspartic hemoglobinase reduces parasite load and blood loss after hookworm infection in dogs. PLoS Med. 2, e295 (2005).
204. Seid, C. A., et al. Expression, purification, characterization of the Necator americanus aspartic protease-1 (Na-APR-1 (M74)) antigen, a component of the bivalent human hookworm vaccine. Hum. Vaccin. Immunother. 11, 1474-1488 (2015).
205. Zhan, B., et al. Molecular cloning, biochemical characterization, partial protective immunity of the heme-binding glutathione S-transferases from the human hookworm Necator americanus. Infect. Immun. 78, 1552-1563 (2010).
206. Loukas, A., et al. Vaccinomics for the major blood feeding helminths of humans. OMICS 15, 567-577 (2011).