• 1

    de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L, 2003. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol 19 :547–551.

    • Search Google Scholar
    • Export Citation
  • 2

    World Health Organization, 2002. The World Health Report 2002: Reducing Risks, Promoting Healthy Life. Geneva: World Health Organization.

  • 3

    Cappello M, Harrison LM, Bungiro RD Jr, Chadderdon RC, Milstone A, Nerlinger A, Kuzmic P, 2003. Molecular pathogenesis of hookworm anemia: prospects for a disease-based vaccine. J Parasitol 89 (Suppl):S158–S164.

    • Search Google Scholar
    • Export Citation
  • 4

    Hotez PJ, Zhan B, Bethony JM, Loukas A, Williamson A, Goud GN, Hawdon JM, Dobardzic A, Dobardzic R, Ghosh K, Bottazzi ME, Mendez S, Zook B, Wang Y, Liu S, Essiet-Gibson I, Chung-Debose S, Xiao S, Knox D, Meagher M, Inan M, Correa-Oliveira R, Vilk P, Shepherd HR, Brandt W, Russell PK, 2003. Progress in the development of a recombinant vaccine for human hookworm disease: the human hookworm vaccine initiative. Int J Parasitol 33 :1245–1258.

    • Search Google Scholar
    • Export Citation
  • 5

    Brooker S, Bethony J, Hotez PJ, 2004. Human hookworm infection in the 21st century. Adv Parasitol 58 :197–288.

  • 6

    Bungiro R, Cappello M, 2004. Hookworm infection: new developments and prospects for control. Curr Opin Infect Dis 17 :421–426.

  • 7

    Booth M, Vounatsou P, N’Goran EK, Tanner M, Utzinger J, 2003. The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Côte d’Ivoire. Parasitology 127 :525–531.

    • Search Google Scholar
    • Export Citation
  • 8

    Anderson RM, Schad GA, 1985. Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Trans R Soc Trop Med Hyg 79 :812–825.

    • Search Google Scholar
    • Export Citation
  • 9

    Hall A, 1981. Quantitative variability of nematode egg counts in faeces: a study among rural Kenyans. Trans R Soc Trop Med Hyg 75 :682–687.

    • Search Google Scholar
    • Export Citation
  • 10

    Ganguly NK, Mahajan RC, Sehgal R, Shetty P, Dilawari JB, 1988. Role of specific immunoglobulin E to excretory-secretory antigen in diagnosis and prognosis of hookworm infection. J Clin Microbiol 26 :739–742.

    • Search Google Scholar
    • Export Citation
  • 11

    Pritchard DI, Walsh EA, 1995. The specificity of the human IgE response to Necator americanus.Parasite Immunol 17 :605–607.

  • 12

    Loukas A, Opdebeeck J, Croese J, Prociv P, 1996. Immunoglobulin G subclass antibodies against excretory/secretory antigens of Ancylostoma caninum in human enteric infections. Am J Trop Med Hyg 54 :672–676.

    • Search Google Scholar
    • Export Citation
  • 13

    Kwon IH, Kim HS, Lee JH, Choi MH, Chai JY, Nakamura-Uchiyama F, Nawa Y, Cho KH, 2003. A serologically diagnosed human case of cutaneous larva migrans caused by Ancylostoma caninum.Korean J Parasitol 41 :233–237.

    • Search Google Scholar
    • Export Citation
  • 14

    Geiger SM, Massara CL, Bethony J, Soboslay PT, Correa-Oliveira R, 2004. Cellular responses and cytokine production in post-treatment hookworm patients from an endemic area in Brazil. Clin Exp Immunol 136 :334–340.

    • Search Google Scholar
    • Export Citation
  • 15

    Pritchard DI, Quinnell RJ, McKean PG, Walsh L, Leggett KV, Slater AF, Raiko A, Dale DD, Keymer AE, 1991. Antigenic cross-reactivity between Necator americanus and Ascaris lumbricoides in a community in Papua New Guinea infected predominantly with hookworm. Trans R Soc Trop Med Hyg 85 :511–514.

    • Search Google Scholar
    • Export Citation
  • 16

    Timothy LM, Coulson PS, Behnke JM, Wilson RA, 1992. Cross-reactivity between Necator americanus and Schistosoma mansoni in mice. Int J Parasitol 22 :1143–1149.

    • Search Google Scholar
    • Export Citation
  • 17

    Bungiro RD Jr, Greene J, Kruglov E, Cappello M, 2001. Mitigation of hookworm disease by immunization with soluble extracts of Ancylostoma ceylanicum.J Infect Dis 183 :1380–1387.

    • Search Google Scholar
    • Export Citation
  • 18

    Bungiro RD, Harrison LM, Cappello M, 2002. Ancylostoma ceylanicum excretory/secretory protein 1: purification and molecular cloning of a major secretory protein from adult hookworms. Mol Biochem Parasitol 119 :147–151.

    • Search Google Scholar
    • Export Citation
  • 19

    Bungiro RD Jr, Anderson BR, Cappello M, 2003. Oral transfer of adult Ancylostoma ceylanicum hookworms into permissive and nonpermissive host species. Infect Immun 71 :1880–1886.

    • Search Google Scholar
    • Export Citation
  • 20

    Bungiro RD Jr, Solis CV, Harrison LM, Cappello M, 2004. Purification and molecular cloning of and immunization with Ancylostoma ceylanicum excretory-secretory protein 2, an immunoreactive protein produced by adult hookworms. Infect Immun 72 :2203–2213.

    • Search Google Scholar
    • Export Citation
  • 21

    Chu D, Bungiro RD, Ibanez M, Harrison LM, Campodonico E, Jones BF, Mieszczanek J, Kuzmic P, Cappello M, 2004. Molecular characterization of Ancylostoma ceylanicum Kunitz-type serine protease inhibitor: evidence for a role in hookworm-associated growth delay. Infect Immun 72 :2214–2221.

    • Search Google Scholar
    • Export Citation
  • 22

    Harrison LM, Nerlinger A, Bungiro RD, Cordova JL, Kuzmic P, Cappello M, 2002. Molecular characterization of Ancylostoma inhibitors of coagulation factor Xa. Hookworm anticoagulant activity in vitro predicts parasite bloodfeeding in vivo.J Biol Chem 277 :6223–6229.

    • Search Google Scholar
    • Export Citation
  • 23

    Milstone AM, Harrison LM, Bungiro RD, Kuzmic P, Cappello M, 2000. A broad spectrum kunitz type serine protease inhibitor secreted by the hookworm Ancylostoma ceylanicum.J Biol Chem 275 :29391–29399.

    • Search Google Scholar
    • Export Citation
  • 24

    Garside P, Behnke JM, 1989. Ancylostoma ceylanicum in the hamster: observations on the host-parasite relationship during primary infection. Parasitology 98 :283–289.

    • Search Google Scholar
    • Export Citation
  • 25

    Ellis TM, Gregory A, Turnor R, Kalkhoven M, Wroth RH, 1993. Detection of Haemonchus contortus surface antigen in faeces from infected sheep. Vet Parasitol 51 :85–97.

    • Search Google Scholar
    • Export Citation
  • 26

    Johnson DA, Behnke JM, Coles GC, 2004. Copro-antigen capture ELISA for the detection of Teladorsagia (Ostertagia) circumcincta in sheep: improvement of specificity by heat treatment. Parasitology 129 :115–126.

    • Search Google Scholar
    • Export Citation
  • 27

    Agneessens J, Claerebout E, Vercruysse J, 2001. Development of a coproantigen capture ELISA for detecting Ostertagia ostertagi infections in cattle. Vet Parasitol 97 :227–238.

    • Search Google Scholar
    • Export Citation
  • 28

    Johnson MJ, Behnke JM, Coles GC, 1996. Detection of gastrointestinal nematodes by a coproantigen capture ELISA. Res Vet Sci 60 :7–12.

  • 29

    Boulos LM, Ibrahim IR, Negm AY, Aly SM, 2001. Detection of coproantigen in early trichinellosis. Parasite 8 (Suppl 2):S136–S139.

  • 30

    Nageswaran C, Craig PS, Devaney E, 1994. Coproantigen detection in rats experimentally infected with Strongyloides ratti.Parasitology 108 :335–342.

    • Search Google Scholar
    • Export Citation
  • 31

    Menon S, Bhopale MK, 1985. Ancylostoma ceylanicum (Looss, 1911) in golden hamsters (Mesocricetus auratus): pathogenicity and humoral immune response to a primary infection. J Helminthol 59 :143–146.

    • Search Google Scholar
    • Export Citation
  • 32

    Stoltzfus RJ, Albonico M, Chwaya HM, Savioli L, Tielsch J, Schulze K, Yip R, 1996. Hemoquant determination of hookworm-related blood loss and its role in iron deficiency in African children. Am J Trop Med Hyg 55 :399–404.

    • Search Google Scholar
    • Export Citation
  • 33

    Bundy DA, Foreman JD, Golden MH, 1985. Sodium azide preservation of faecal specimens for Kato analysis. Parasitology 90 :463–469.

  • 34

    Foreyt WJ, 1986. Recovery of nematode eggs and larvae in deer: evaluation of fecal preservation methods. J Am Vet Med Assoc 189 :1065–1067.

    • Search Google Scholar
    • Export Citation
  • 35

    Allan JC, Mencos F, Garcia-Noval J, Sarti E, Flisser A, Wang Y, Liu D, Craig PS, 1993. Dipstick dot ELISA for the detection of Taenia coproantigens in humans. Parasitology 107 :79–85.

    • Search Google Scholar
    • Export Citation
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

DETECTION OF EXCRETORY/SECRETORY COPROANTIGENS IN EXPERIMENTAL HOOKWORM INFECTION

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  • 1 Program in International Child Health, Department of Pediatrics, Yale University School of Medicine, New Haven, Connecticut

This report describes the detection of hookworm excretory/secretory (ES) antigens in soluble hamster fecal extracts by an enzyme-linked immunosorbent assay (ELISA). A rabbit polyclonal IgG antibody against Ancylostoma ceylanicum ES was used to capture hookworm coproantigens that were then detected using pooled, high-titer, infected hamster serum. The ELISA was capable of detecting ES proteins over a range of 10 ng/mL to 10 μg/mL when the antigens were diluted in buffer or uninfected fecal extract, and ES could be detected in infected hamster feces at dilutions up to 1:256. Examination of the kinetics of coproantigen production demonstrated that detectable amounts of ES were produced as early as four days after A. ceylanicum infection, whereas fecal eggs were not observed until day 17. Moreover, fecal ES levels correlated well with intestinal worm burden and could be detected in wet or dry stool samples stored for 14 days over a temperature range of −80°C to 37°C. The fecal ELISA was then adapted to analyze the excretion of AceES-2, a novel immunogenic ES protein recently cloned from A. ceylanicum cDNA. AceES-2 was found to be excreted in feces with kinetics similar to that of whole ES. Examination of individual hookworm antigens by this method will provide new insights into the molecular host-parasite interaction and may form the basis for future diagnostic methods.

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