Keiser J, Utzinger J, 2008. Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA 299: 1937–1948.
Keiser J, Utzinger J, 2010. The drugs we have and the drugs we need against major helminth infections. Adv Parasitol 73: 197–230.
Geerts S, Gryseels B, 2000. Drug resistance in human helminths: current situation and lessons from livestock. Clin Microbiol Rev 13: 207–222.
Kaplan RM, 2004. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol 20: 477–481.
Demeler J, Kleinschmidt N, Küttler U, Koopmann R, von Samson-Himmelstjerna G, 2012. Evaluation of the egg hatch assay and the larval migration inhibition assay to detect anthelmintic resistance in cattle parasitic nematodes on farms. Parasitol Int 61: 614–618.
Albonico M, Wright V, Ramsan M, Haji HJ, Taylor M, Savioli L, Bickle Q, 2005. Development of the egg hatch assay for detection of anthelmintic resistance in human hookworms. Int J Parasitol 35: 803–811.
Kotze AC, Lowe A, O'Grady J, Kopp SR, Behnke JM, 2009. Dose-response assay templates for in vitro assessment of resistance to benzimidazole and nicotinic acetylcholine receptor agonist drugs in human hookworms. Am J Trop Med Hyg 81: 163–170.
Cappello M, Bungiro RD, Harrison LM, Bischof LJ, Griffitts JS, Barrows BD, Aroian RV, 2006. A purified Bascillus thuringiensis crystal protein with therapeutic activity against the hookworm parasite Ancylostoma ceylanicum. Proc Natl Acad Sci USA 103: 15154–15159.
Vermeire JJ, Lantz L, Caffrey CR, 2012. Cure of hookworm infection with a cysteine protease inhibitor. PLoS Negl Trop Dis 6: e1680.
Koné WM, Vargas M, Keiser J, 2012. Anthelmintic activity of medicinal plants used in Côte d'Ivoire for treating parasitic diseases. Parasitol Res 110: 2351–2362.
Xue J, Xiao SH, Xu LL, Qiang HQ, 2010. The effect of tribendimidine and its metabolites against Necator americanus in golden hamsters and Nippostrongylus braziliensis in rats. Parasitol Res 106: 775–781.
Harder A, Schmitt-Wrede HP, Krücken J, Marinovski P, Wunderlich F, Willson J, Amliwala K, Holden-Dye L, Walker R, 2003. Cyclooctadepsipeptides–an anthelmintically active class of compounds exhibiting a novel mode of action. Int J Antimicrob Agents 22: 318–331.
Tritten L, Silbereisen A, Keiser J, 2011. In vitro and in vivo efficacy of Monepantel (AAD 1566) against laboratory models of human intestinal nematode infections. PLoS Negl Trop Dis 5: e1457.
Keiser J, Vargas M, Winter R, 2012. Anthelmintic properties of mangostin and mangostin diacetate. Parasitol Int 61: 369–371.
Tritten L, Braissant O, Keiser J, 2012. Comparison of novel and existing tools for studying drug sensitivity against the hookworm Ancylostoma ceylanicum in vitro. Parasitology 139: 348–357.
Tritten L, Nwosu U, Vargas M, Keiser J, 2012. In vitro and in vivo efficacy of tribendimidine and its metabolites alone and in combination against the hookworms Heligmosomoides bakeri and Ancylostoma ceylanicum. Acta Trop 122: 101–107.
Szewczuk VD, Mongelli ER, Pomilio AB, 2006. In vitro anthelmintic activity of melia azedarach naturalized in Argentina. Phytother Res 20: 993–996.
Wolpert BJ, Beauvoir MG, Wells EF, Hawdon JM, 2008. Plant vermicides of Haitian Vodou show in vitro activity against larval hookworm. J Parasitol 94: 1155–1160.
Colgrave ML, Kotze AC, Kopp S, McCarthy JS, Coleman GT, Craik DJ, 2009. Anthelmintic activity of cyclotides: in vitro studies with canine and human hookworms. Acta Trop 109: 163–166.
Fred-Jaiyesimi AA, Adepoju A, Egbebunmi O, 2011. Anthelmintic activities of chloroform and methanol extracts of Buchholzia coriacea Engler seed. Parasitol Res 109: 441–444.
De Clercq D, Sacko M, Behnke J, Gilbert F, Dorny P, Vercruysse J, 1997. Failure of mebendazole in treatment of human hookworm infections in the southern region of Mali. Am J Trop Med Hyg 57: 25–30.
Kotze AC, Coleman GT, Mai A, McCarthy JS, 2005. Field evaluation of anthelmintic drug sensitivity using in vitro egg hatch and larval motility assays with Necator americanus recovered from human field isolates. Int J Parasitol 35: 445–453.
Kotze AC, Steinmann P, Zhou H, Du ZW, Zhou XN, 2011. The effect of egg embryonation on field-use of a hookworm benzimidazole-sensitivity egg hatch assay in Yunnan Province, People's Republic of China. PLoS Negl Trop Dis 5: e1203.
Hoekstra R, Borgsteede FH, Boersema JH, Roos MH, 1997. Selection for high levamisole resistance in Haemonchus contortus monitored with an egg-hatch assay. Int J Parasitol 27: 1395–1400.
Várady M, Bjørn H, Craven J, Nansen P, 1997. In vitro characterization of lines of Oesophagostomum dentatum selected or not selected for resistance to pyrantel, levamisole and ivermectin. Int J Parasitol 27: 77–81.
Treger RS, Cook A, Rai G, Maloney DJ, Simeonov A, Jadhav A, Thomas CJ, Williams DL, Cappello M, Vermeire JJ, 2012. Oxadiazole 2-oxides are toxic to the human hookworm, Ancylostoma ceylanicum, however glutathione reductase is not the primary target. Int J Parasitol Drugs Drug Resist 2: 171–177.
Rai G, Sayed AA, Lea WA, Luecke HF, Chakrapani H, Prast-Nielsen S, Jadhav A, Leister W, Shen M, Inglese J, Austin CP, Keefer L, Arnér ES, Simeonov A, Maloney DJ, Williams DL, Thomas CJ, 2009. Structure mechanism insights and the role of nitric oxide donation guide the development of oxadiazole-2-oxides as therapeutic agents against schistosomiasis. J Med Chem 52: 6474–6483.
Lee EF, Clarke OB, Evangelista M, Feng Z, Speed TP, Tchoubrieva EB, Strasser A, Kalinna BH, Colman PM, Fairlie WD, 2011. Discovery and molecular characterization of a Bcl-2-regulated cell death pathway in schistosomes. Proc Natl Acad Sci USA 108: 6999–7003.
Coles GC, Bauer C, Borgsteede FH, Geerts S, Klei TR, Taylor MA, Waller PJ, 1992. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 44: 35–44.
Reiss D, Harrison LM, Bungiro R, Cappello M, 2007. Short report: an agar plate method for culturing hookworm larvae: analysis of growth kinetics and infectivity compared with standard coproculture techniques. Am J Trop Med Hyg 77: 1087–1090.
Humphries D, Mosites E, Otchere J, Twum WA, Woo L, Jones-Sanpei H, Harrison LM, Bungiro RD, Benham-Pyle B, Bimi L, Edoh D, Bosompem K, Wilson M, Cappello M, 2011. Epidemiology of hookworm infection in Kintampo North Municipality, Ghana: patterns of malaria coinfection, anemia, and albendazole treatment failure. Am J Trop Med Hyg 84: 792–800.
Katz N, Chaves A, Pellegrino J, 1972. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397–400.
Horton J, 2000. Albendazole: a review of anthelmintic efficacy and safety in humans. Parasitology 121: S113–S132.
Albonico M, Stoltzfus RJ, Savioli L, Tielsch JM, Chwaya HM, Ercole E, Cancrini G, 1998. 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.
Hotez PJ, Bethony JM, Diemert DJ, Pearson M, Loukas A, 2010. Developing vaccines to combat hookworm infection and intestinal schistosomiasis. Nat Rev Microbiol 8: 814–826.
de Gruijter JM, van Lieshout L, Gasser RB, Verweij JJ, Brienen EA, Ziem JB, Yelifari L, Polderman AM, 2005. Polymerase chain reaction-based differential diagnosis of Ancylostoma duodenale and Necator americanus infections in humans in northern Ghana. Trop Med Int Health 10: 574–580.
Verweij JJ, Brienen EA, Ziem J, Yelifari L, Polderman AM, Van Lieshout L, 2007. Simultaneous detection and quantification of Ancylostoma duodenale, Necator americanus, and Oesophagostomum bifurcum in fecal samples using multiplex real-time PCR. Am J Trop Med Hyg 77: 685–690.
Kotze AC, Clifford S, O'Grady J, Behnke JM, McCarthy JS, 2004. An in vitro larval motility assay to determine anthelmintic sensitivity for human hookworm and Strongyloides species. Am J Trop Med Hyg 71: 608–616.
Richards JC, Behnke JM, Duce IR, 1995. In vitro studies on the relative sensitivity to ivermectin of Necator americanus and Ancylostoma ceylanicum. Int J Parasitol 25: 1185–1191.
Behnke JM, Rose R, Garside P, 1993. Sensitivity to ivermectin and pyrantel of Ancylostoma ceylanicum and Necator americanus. Int J Parasitol 23: 945–952.
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Abstract Views | 2463 | 2370 | 87 |
Full Text Views | 309 | 17 | 3 |
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A panel of 80 compounds was screened for anthelmintic activity against a laboratory strain of Ancylostoma ceylanicum and field isolates of hookworm obtained from school children in the Kintampo North District of the Brong Ahafo Region of Ghana. Although the laboratory strain of A. ceylanicum was more susceptible to the compounds tested than the field isolates of hookworm, a twofold increase in compound concentration resulted in comparable egg hatch percent inhibition for select compounds. These data provide evidence that the efficacy of anthelmintic compounds may be species-dependent and that field and laboratory strains of hookworm differ in their sensitivities to the anthelmintics tested. These data also suggest that both compound concentration and hookworm species must be considered when screening to identify novel anthelmintic compounds.
Financial support: This work was supported by National Institutes of Health Chemical Genomics Center Contract HHSN268201000217P (to M.C. and J.J.V.), National Institutes of Health Career Development Award K22 A08476 (to J.J.V.), the Noguchi Memorial Institute for Medical Research, and the Yale–Ghana Partnership in Global Health.
Authors' addresses: Rebecca S. Treger, Department of Pediatrics and Program in International Child Health, Yale University School of Medicine, New Haven, CT, E-mail: rebecca.treger@yale.edu. Joseph Otchere, Josephine E. Quagraine, and Michael Wilson, Noguchi Memorial Institute for Medical Research, University of Ghana, Legon, Ghana, E-mails: jotchere@noguchi.mimcom.org, jquagraine@noguchi.mimcom.org, and mwilson@noguchi.mimcom.org. Martin F. Keil and Debbie L. Humphries, Yale School of Public Health, Yale University, New Haven, CT, E-mails: martin.keil@yale.edu and debbie.humphries@yale.edu. Ganesha Rai and Bryan T. Mott, National Institutes of Health Chemical Genomics Center, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, E-mails: bantukallug@mail.nih.gov and bryan.mott@nih.gov. Michael Cappello and Jon J. Vermeire, Yale Child Health Research Center, Yale University, New Haven, CT, E-mails: michael.cappello@yale.edu and jon.vermeire@yale.edu.
Keiser J, Utzinger J, 2008. Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA 299: 1937–1948.
Keiser J, Utzinger J, 2010. The drugs we have and the drugs we need against major helminth infections. Adv Parasitol 73: 197–230.
Geerts S, Gryseels B, 2000. Drug resistance in human helminths: current situation and lessons from livestock. Clin Microbiol Rev 13: 207–222.
Kaplan RM, 2004. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol 20: 477–481.
Demeler J, Kleinschmidt N, Küttler U, Koopmann R, von Samson-Himmelstjerna G, 2012. Evaluation of the egg hatch assay and the larval migration inhibition assay to detect anthelmintic resistance in cattle parasitic nematodes on farms. Parasitol Int 61: 614–618.
Albonico M, Wright V, Ramsan M, Haji HJ, Taylor M, Savioli L, Bickle Q, 2005. Development of the egg hatch assay for detection of anthelmintic resistance in human hookworms. Int J Parasitol 35: 803–811.
Kotze AC, Lowe A, O'Grady J, Kopp SR, Behnke JM, 2009. Dose-response assay templates for in vitro assessment of resistance to benzimidazole and nicotinic acetylcholine receptor agonist drugs in human hookworms. Am J Trop Med Hyg 81: 163–170.
Cappello M, Bungiro RD, Harrison LM, Bischof LJ, Griffitts JS, Barrows BD, Aroian RV, 2006. A purified Bascillus thuringiensis crystal protein with therapeutic activity against the hookworm parasite Ancylostoma ceylanicum. Proc Natl Acad Sci USA 103: 15154–15159.
Vermeire JJ, Lantz L, Caffrey CR, 2012. Cure of hookworm infection with a cysteine protease inhibitor. PLoS Negl Trop Dis 6: e1680.
Koné WM, Vargas M, Keiser J, 2012. Anthelmintic activity of medicinal plants used in Côte d'Ivoire for treating parasitic diseases. Parasitol Res 110: 2351–2362.
Xue J, Xiao SH, Xu LL, Qiang HQ, 2010. The effect of tribendimidine and its metabolites against Necator americanus in golden hamsters and Nippostrongylus braziliensis in rats. Parasitol Res 106: 775–781.
Harder A, Schmitt-Wrede HP, Krücken J, Marinovski P, Wunderlich F, Willson J, Amliwala K, Holden-Dye L, Walker R, 2003. Cyclooctadepsipeptides–an anthelmintically active class of compounds exhibiting a novel mode of action. Int J Antimicrob Agents 22: 318–331.
Tritten L, Silbereisen A, Keiser J, 2011. In vitro and in vivo efficacy of Monepantel (AAD 1566) against laboratory models of human intestinal nematode infections. PLoS Negl Trop Dis 5: e1457.
Keiser J, Vargas M, Winter R, 2012. Anthelmintic properties of mangostin and mangostin diacetate. Parasitol Int 61: 369–371.
Tritten L, Braissant O, Keiser J, 2012. Comparison of novel and existing tools for studying drug sensitivity against the hookworm Ancylostoma ceylanicum in vitro. Parasitology 139: 348–357.
Tritten L, Nwosu U, Vargas M, Keiser J, 2012. In vitro and in vivo efficacy of tribendimidine and its metabolites alone and in combination against the hookworms Heligmosomoides bakeri and Ancylostoma ceylanicum. Acta Trop 122: 101–107.
Szewczuk VD, Mongelli ER, Pomilio AB, 2006. In vitro anthelmintic activity of melia azedarach naturalized in Argentina. Phytother Res 20: 993–996.
Wolpert BJ, Beauvoir MG, Wells EF, Hawdon JM, 2008. Plant vermicides of Haitian Vodou show in vitro activity against larval hookworm. J Parasitol 94: 1155–1160.
Colgrave ML, Kotze AC, Kopp S, McCarthy JS, Coleman GT, Craik DJ, 2009. Anthelmintic activity of cyclotides: in vitro studies with canine and human hookworms. Acta Trop 109: 163–166.
Fred-Jaiyesimi AA, Adepoju A, Egbebunmi O, 2011. Anthelmintic activities of chloroform and methanol extracts of Buchholzia coriacea Engler seed. Parasitol Res 109: 441–444.
De Clercq D, Sacko M, Behnke J, Gilbert F, Dorny P, Vercruysse J, 1997. Failure of mebendazole in treatment of human hookworm infections in the southern region of Mali. Am J Trop Med Hyg 57: 25–30.
Kotze AC, Coleman GT, Mai A, McCarthy JS, 2005. Field evaluation of anthelmintic drug sensitivity using in vitro egg hatch and larval motility assays with Necator americanus recovered from human field isolates. Int J Parasitol 35: 445–453.
Kotze AC, Steinmann P, Zhou H, Du ZW, Zhou XN, 2011. The effect of egg embryonation on field-use of a hookworm benzimidazole-sensitivity egg hatch assay in Yunnan Province, People's Republic of China. PLoS Negl Trop Dis 5: e1203.
Hoekstra R, Borgsteede FH, Boersema JH, Roos MH, 1997. Selection for high levamisole resistance in Haemonchus contortus monitored with an egg-hatch assay. Int J Parasitol 27: 1395–1400.
Várady M, Bjørn H, Craven J, Nansen P, 1997. In vitro characterization of lines of Oesophagostomum dentatum selected or not selected for resistance to pyrantel, levamisole and ivermectin. Int J Parasitol 27: 77–81.
Treger RS, Cook A, Rai G, Maloney DJ, Simeonov A, Jadhav A, Thomas CJ, Williams DL, Cappello M, Vermeire JJ, 2012. Oxadiazole 2-oxides are toxic to the human hookworm, Ancylostoma ceylanicum, however glutathione reductase is not the primary target. Int J Parasitol Drugs Drug Resist 2: 171–177.
Rai G, Sayed AA, Lea WA, Luecke HF, Chakrapani H, Prast-Nielsen S, Jadhav A, Leister W, Shen M, Inglese J, Austin CP, Keefer L, Arnér ES, Simeonov A, Maloney DJ, Williams DL, Thomas CJ, 2009. Structure mechanism insights and the role of nitric oxide donation guide the development of oxadiazole-2-oxides as therapeutic agents against schistosomiasis. J Med Chem 52: 6474–6483.
Lee EF, Clarke OB, Evangelista M, Feng Z, Speed TP, Tchoubrieva EB, Strasser A, Kalinna BH, Colman PM, Fairlie WD, 2011. Discovery and molecular characterization of a Bcl-2-regulated cell death pathway in schistosomes. Proc Natl Acad Sci USA 108: 6999–7003.
Coles GC, Bauer C, Borgsteede FH, Geerts S, Klei TR, Taylor MA, Waller PJ, 1992. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 44: 35–44.
Reiss D, Harrison LM, Bungiro R, Cappello M, 2007. Short report: an agar plate method for culturing hookworm larvae: analysis of growth kinetics and infectivity compared with standard coproculture techniques. Am J Trop Med Hyg 77: 1087–1090.
Humphries D, Mosites E, Otchere J, Twum WA, Woo L, Jones-Sanpei H, Harrison LM, Bungiro RD, Benham-Pyle B, Bimi L, Edoh D, Bosompem K, Wilson M, Cappello M, 2011. Epidemiology of hookworm infection in Kintampo North Municipality, Ghana: patterns of malaria coinfection, anemia, and albendazole treatment failure. Am J Trop Med Hyg 84: 792–800.
Katz N, Chaves A, Pellegrino J, 1972. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397–400.
Horton J, 2000. Albendazole: a review of anthelmintic efficacy and safety in humans. Parasitology 121: S113–S132.
Albonico M, Stoltzfus RJ, Savioli L, Tielsch JM, Chwaya HM, Ercole E, Cancrini G, 1998. 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.
Hotez PJ, Bethony JM, Diemert DJ, Pearson M, Loukas A, 2010. Developing vaccines to combat hookworm infection and intestinal schistosomiasis. Nat Rev Microbiol 8: 814–826.
de Gruijter JM, van Lieshout L, Gasser RB, Verweij JJ, Brienen EA, Ziem JB, Yelifari L, Polderman AM, 2005. Polymerase chain reaction-based differential diagnosis of Ancylostoma duodenale and Necator americanus infections in humans in northern Ghana. Trop Med Int Health 10: 574–580.
Verweij JJ, Brienen EA, Ziem J, Yelifari L, Polderman AM, Van Lieshout L, 2007. Simultaneous detection and quantification of Ancylostoma duodenale, Necator americanus, and Oesophagostomum bifurcum in fecal samples using multiplex real-time PCR. Am J Trop Med Hyg 77: 685–690.
Kotze AC, Clifford S, O'Grady J, Behnke JM, McCarthy JS, 2004. An in vitro larval motility assay to determine anthelmintic sensitivity for human hookworm and Strongyloides species. Am J Trop Med Hyg 71: 608–616.
Richards JC, Behnke JM, Duce IR, 1995. In vitro studies on the relative sensitivity to ivermectin of Necator americanus and Ancylostoma ceylanicum. Int J Parasitol 25: 1185–1191.
Behnke JM, Rose R, Garside P, 1993. Sensitivity to ivermectin and pyrantel of Ancylostoma ceylanicum and Necator americanus. Int J Parasitol 23: 945–952.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 2463 | 2370 | 87 |
Full Text Views | 309 | 17 | 3 |
PDF Downloads | 107 | 17 | 1 |