Author:
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2016. Progress towards eliminating onchocerciasis in the WHO Region of the Americas: verification of elimination of transmission in Guatemala. Wkly Epidemiol Rec 91: 501–504.
-
2.
Allen JE et al. 2008. Of mice, cattle, and humans: the immunology and treatment of river blindness. PLoS Negl Trop Dis 2: e217.
-
3.
Abraham D, Lucius R, Trees AJ, 2002. Immunity to Onchocerca spp. in animal hosts. Trends Parasitol 18: 164–171.
-
4.
Lovato R, Guevara A, Guderian R, Proano R, Unnasch T, Criollo H, Hassan HK, Mackenzie CD, 2014. Interruption of infection transmission in the onchocerciasis focus of Ecuador leading to the cessation of ivermectin distribution. PLoS Negl Trop Dis 8: e2821.
-
5.
Rodriguez-Perez MA, Dominguez-Vazquez A, Unnasch TR, Hassan HK, Arredondo-Jimenez JI, Orozco-Algarra ME, Rodriguez-Morales KB, Rodriguez-Luna IC, Prado-Velasco FG, 2013. Interruption of transmission of Onchocerca volvulus in the southern Chiapas Focus, Mexico. PLoS Negl Trop Dis 7: e2133.
-
6.
Gonzalez RJ et al. 2009. Successful interruption of transmission of Onchocerca volvulus in the Escuintla-Guatemala Focus, Guatemala. PLoS Negl Trop Dis 3: e404.
-
7.
Lindblade KA et al. 2007. Elimination of Onchocercia volvulus transmission in the Santa Rosa focus of Guatemala. Am J Trop Med Hyg 77: 334–341.
-
8.
World Health Organization, 2013. Progress towards eliminating onchocerciasis in the WHO Region of the Americas: verification by WHO of elimination of transmission in Colombia. Wkly Epidemiol Rec 88: 381–385.
-
9.
Higazi TB et al. 2013. Interruption of Onchocerca volvulus transmission in the Abu Hamed Focus, Sudan. Am J Trop Med Hyg 89: 51–57.
-
10.
Katabarwa M et al. 2014. Transmission of Onchocerca volvulus by Simulium neavei in Mount Elgon focus of eastern Uganda has been interrupted. Am J Trop Med Hyg 90: 1159–1166.
-
11.
Oguttu D et al. 2014. Serosurveillance to monitor onchocerciasis elimination: the Ugandan experience. Am J Trop Med Hyg 90: 339–345.
-
12.
World Health Organization, 2014. Elimination of onchocerciasis in the WHO region of the Americas: Ecuador’s progress towards verification of elimination. Wkly Epidemiol Rec 89: 401–405.
-
13.
World Health Organization, 2015. Progress toward eliminating onchocerciasis in the WHO region of the Americas: verification of elimination of transmission in Mexico. Wkly Epidemiol Rec 90: 577–581.
-
14.
World Health Organization, 2010. African programme for onchocerciasis control—report of the sixth meeting of National Task Forces, October 2009. Wkly Epidemiol Rec 85: 23–28.
-
15.
World Health Organization, 1995. Onchocerciasis and its control. Report of a WHO expert committee on onchocerciasis control. World Health Organ Tech Rep Ser 852: 1–104.
-
16.
Bottomley C, Isham V, Vivas-Martinez S, Kuesel AC, Attah SK, Opoku NO, Lustigman S, Walker M, Basanez MG, 2016. Modelling neglected tropical diseases diagnostics: the sensitivity of skin snips for Onchocerca volvulus in near elimination and surveillance settings. Parasit Vectors 9: 343.
-
17.
Thiele EA, Cama VA, Lakwo T, Mekasha S, Abanyie F, Sleshi M, Kebede A, Cantey PT, 2016. Detection of Onchocerca volvulus in skin snips by microscopy and real-time polymerase chain reaction: implications for monitoring and evaluation activities. Am J Trop Med Hyg 94: 906–911.
-
18.
Toe L, Boatin BA, Adjami A, Back C, Merriweather A, Unnasch TR, 1998. Detection of Onchocerca volvulus infection by O-150 polymerase chain reaction analysis of skin scratches. J Infect Dis 178: 282–285.
-
19.
Lobos E, Altmann M, Mengod G, Weiss N, Rudin W, Karam M, 1990. Identification of an Onchocerca volvulus cDNA encoding a low-molecular-weight antigen uniquely recognized by onchocerciasis patient sera. Mol Biochem Parasitol 39: 135–145.
-
20.
Lobos E, Weiss N, Karam M, Taylor HR, Ottesen EA, Nutman TB, 1991. An immunogenic Onchocerca volvulus antigen: a specific and early marker of infection. Science 251: 1603–1605.
-
21.
Lazzeri M, Nutman T, Weiss N, 1995. Nucleotide Molecule Enconding a Specific Onchocerca volvulus Antigen for the Immunodiagnosis of onchocerciasis. USPTO, ed. Washington, DC: United Stated Patent and Trademark Office. United States Patent Number: 5,416,009.
-
22.
Ogunrinade AF, Awolola SO, Rotimi O, Chandrashekar R, 2000. Longitudinal studies of skin microfilaria and antibody conversion rates in children living in an endemic focus of onchocerciasis in Nigeria. J Trop Pediatr 46: 348–351.
-
23.
Rodriguez-Perez MA, Unnasch TR, Dominguez-Vazquez A, Morales-Castro AL, Pena-Flores GP, Orozco-Algarra ME, Arredondo-Jimenez JI, Richards F Jr., Vasquez-Rodriguez MA, Rendon VG, 2010. Interruption of transmission of Onchocerca volvulus in the Oaxaca focus, Mexico. Am J Trop Med Hyg 83: 21–27.
-
24.
Zarroug IM et al. 2016. The first confirmed elimination of an onchocerciasis focus in Africa: Abu Hamed, Sudan. Am J Trop Med Hyg 95: 1037–1040.
-
25.
Eberhard ML, Dickerson JW, Boyer AE, Tsang VC, Zea-Flores R, Walker EM, Richards FO, Zea-Flores G, Strobert E, 1991. Experimental Onchocerca volvulus infections in mangabey monkeys (Cercocebus atys) compared to infections in humans and chimpanzees (Pan troglodytes). Am J Trop Med Hyg 44: 151–160.
-
26.
Eberhard ML et al. 1995. Onchocerca volvulus: parasitologic and serologic responses in experimentally infected chimpanzees and mangabey monkeys. Exp Parasitol 80: 454–462.
-
27.
Abraham D, Lange AM, Yutanawiboonchai W, Trpis M, Dickerson JW, Swenson B, Eberhard ML, 1993. Survival and development of larval Onchocerca volvulus in diffusion chambers implanted in primate and rodent hosts. J Parasitol 79: 571–582.
-
28.
Cruz-Ortiz N, Gonzalez RJ, Lindblade KA, Richards FO Jr., Sauerbrey M, Zea-Flores G, Dominguez A, Oliva O, Catu E, Rizzo N, 2012. Elimination of Onchocerca volvulus transmission in the Huehuetenango focus of Guatemala. J Parasitol Res 2012: 638429.
-
29.
Press WH, Flannery BP, Teukolski SA, Vetterling WT, 1988. Numerical Recipes in C: The Art of Scientific Computing. New York, NY: Cambridge University Press.
-
30.
Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, Muller M, 2011. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 12: 77.
-
31.
Burbelo PD, Leahy HP, Iadarola MJ, Nutman TB, 2009. A four-antigen mixture for rapid assessment of Onchocerca volvulus infection. PLoS Negl Trop Dis 3: e438.
-
32.
Golden A et al. 2013. Extended result reading window in lateral flow tests detecting exposure to Onchocerca volvulus: a new technology to improve epidemiological surveillance tools. PLoS One 8: e69231.
-
33.
Gass K, 2018. Rethinking the serological threshold for onchocerciasis elimination. PLoS Negl Trop Dis 12: e0006249.
-
34.
Boyer AE, Tsang VC, Eberhard ML, Zea-Flores G, Hightower A, Pilcher JB, Zea-Flores R, Zhou W, Reimer CB, 1991. Guatemalan human onchocerciasis. II. Evidence for IgG3 involvement in acquired immunity to Onchocerca volvulus and identification of possible immune-associated antigens. J Immunol 146: 4001–4010.
-
35.
Tsang VC, Boyer AE, Pilcher JB, Eberhard ML, Reimer CB, Zea-Flores G, Zea-Flores R, Zhou W, Richards FO, 1991. Guatemalan human onchocerciasis. I. Systematic analysis of patient populations, nodular antigens, and specific isotypic reactions. J Immunol 146: 3993–4000.
-
36.
Weiss N, 1986. Immunological approaches to the detection of prepatent onchocerciasis. J Commun Dis 18: 254–260.
-
37.
Henry NL, Law M, Nutman TB, Klion AD, 2001. Onchocerciasis in a nonendemic population: clinical and immunologic assessment before treatment and at the time of presumed cure. J Infect Dis 183: 512–516.
-
38.
Evans DS et al. 2014. Status of Onchocerciasis transmission after more than a decade of mass drug administration for onchocerciasis and lymphatic filariasis elimination in central Nigeria: challenges in coordinating the stop MDA decision. PLoS Negl Trop Dis 8: e3113.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 3871 | 3300 | 212 |
| Full Text Views | 1146 | 21 | 2 |
| PDF Downloads | 255 | 22 | 0 |
Evaluation of an OV-16 IgG4 Enzyme-Linked Immunosorbent Assay in Humans and Its Application to Determine the Dynamics of Antibody Responses in a Non-Human Primate Model of Onchocerca volvulus Infection
Vitaliano A. Cama
Vitaliano A. Cama
Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Circe McDonald
Circe McDonald
Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
IHRC Inc., Atlanta, Georgia;
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IHRC Inc., Atlanta, Georgia;
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Alice Arcury-Quandt
Alice Arcury-Quandt
Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Mark Eberhard
Mark Eberhard
Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
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M. Harley Jenks
M. Harley Jenks
Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
IHRC Inc., Atlanta, Georgia;
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Jared Smith
Jared Smith
Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
IHRC Inc., Atlanta, Georgia;
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Sindew M. Feleke
Sindew M. Feleke
Ethiopian Public Health Institute, Addis Ababa, Ethiopia;
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Francisca Abanyie
Francisca Abanyie
Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Lakwo Thomson
Lakwo Thomson
Vector Control Division, Uganda Ministry of Health, Kampala, Uganda
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Ryan E. Wiegand
Ryan E. Wiegand
Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Paul T. Cantey
Paul T. Cantey
Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Onchocerciasis is a neglected parasitic disease targeted for elimination. Current World Health Organization guidelines for elimination include monitoring antibody responses to the recombinant Onchocerca volvulus antigen OV-16 in children to demonstrate the absence of transmission. We report the performance characteristics of a modified OV-16 enzyme-linked immunosorbent assay (ELISA) and describe anti–OV-16 responses in serum samples from laboratory-inoculated nonhuman primates (NHPs) in relation to microfilariae (mf) in skin snip biopsies. This OV-16 IgG4 ELISA had sensitivity and specificity of 88.2% and 99.7%, respectively, as determined by receiver operator characteristic analysis using a serum panel of 110 positive and 287 negative samples from people infected with other filariae or other parasitic infections. Anti–OV-16 responses in inoculated NHP (N = 9) were evaluated at quarterly intervals for IgM and the four IgG subclasses. Enzyme-linked immunosorbent assay results showed a well-defined IgG4 reactivity pattern and moderate IgG1 antibody responses. Meanwhile, the reactivity by IgG2, IgG3, or IgM did not show a clear pattern. Temporal evolution of IgG4 reactivity was evaluated through monthly testing, showing that NHPs developed anti–OV-16 IgG4 on average at 15 months postinoculation (range: 10–18 months). The average time to detectable mf was also 15 months (range: 11–25). The OV-16 ELISA used in this study was robust and allowed the detection of IgG4 responses, which were observed only among animals with detectable mf (N = 5), four of which showed declines in antibody responses once mf cleared. These findings also confirmed that the most informative antibody subclass responses to OV-16 are IgG4.
- Supplemental Materials (PDF 195 KB)
Author Notes
Financial support: This work was funded in part by CDC and the Bill & Melinda Gates Foundation, grant number OPP1017858.
Authors’ addresses: Vitaliano A. Cama, Circe McDonald, Alice Arcury-Quandt, Mark Eberhard, M. Harley Jenks, Jared Smith, and Ryan E. Wiegand, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: vcama@cdc.gov, circemcd@gmail.com, alice.aq@gmail.com, mle1@cdc.gov, uwq1@cdc.gov, smithjaluga@gmail.com, and fwk2@cdc.gov. Sindew M. Feleke, Malaria and Other Parasitic Disease Research Team, Ethiopia Public Health Institute, Addis Ababa, Ethiopia, E-mail: mekashasindeaw@yahoo.com. Francisca Abanyie, Division of Healthcare Quality and Promotion, Centers for Disease Control and Prevention, Atlanta, GA, E-mail: why6@cdc.gov. Lakwo Thomson, Vector Control Division, Uganda Ministry of Health, Kampala, Uganda, E-mail: tlakwo@gmail.com. Paul T. Cantey, Department of Control of Neglected Tropical Diseases, World Health Organization, Geneva, Switzerland, E-mail: canteyp@who.int.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2016. Progress towards eliminating onchocerciasis in the WHO Region of the Americas: verification of elimination of transmission in Guatemala. Wkly Epidemiol Rec 91: 501–504.
-
2.
Allen JE et al. 2008. Of mice, cattle, and humans: the immunology and treatment of river blindness. PLoS Negl Trop Dis 2: e217.
-
3.
Abraham D, Lucius R, Trees AJ, 2002. Immunity to Onchocerca spp. in animal hosts. Trends Parasitol 18: 164–171.
-
4.
Lovato R, Guevara A, Guderian R, Proano R, Unnasch T, Criollo H, Hassan HK, Mackenzie CD, 2014. Interruption of infection transmission in the onchocerciasis focus of Ecuador leading to the cessation of ivermectin distribution. PLoS Negl Trop Dis 8: e2821.
-
5.
Rodriguez-Perez MA, Dominguez-Vazquez A, Unnasch TR, Hassan HK, Arredondo-Jimenez JI, Orozco-Algarra ME, Rodriguez-Morales KB, Rodriguez-Luna IC, Prado-Velasco FG, 2013. Interruption of transmission of Onchocerca volvulus in the southern Chiapas Focus, Mexico. PLoS Negl Trop Dis 7: e2133.
-
6.
Gonzalez RJ et al. 2009. Successful interruption of transmission of Onchocerca volvulus in the Escuintla-Guatemala Focus, Guatemala. PLoS Negl Trop Dis 3: e404.
-
7.
Lindblade KA et al. 2007. Elimination of Onchocercia volvulus transmission in the Santa Rosa focus of Guatemala. Am J Trop Med Hyg 77: 334–341.
-
8.
World Health Organization, 2013. Progress towards eliminating onchocerciasis in the WHO Region of the Americas: verification by WHO of elimination of transmission in Colombia. Wkly Epidemiol Rec 88: 381–385.
-
9.
Higazi TB et al. 2013. Interruption of Onchocerca volvulus transmission in the Abu Hamed Focus, Sudan. Am J Trop Med Hyg 89: 51–57.
-
10.
Katabarwa M et al. 2014. Transmission of Onchocerca volvulus by Simulium neavei in Mount Elgon focus of eastern Uganda has been interrupted. Am J Trop Med Hyg 90: 1159–1166.
-
11.
Oguttu D et al. 2014. Serosurveillance to monitor onchocerciasis elimination: the Ugandan experience. Am J Trop Med Hyg 90: 339–345.
-
12.
World Health Organization, 2014. Elimination of onchocerciasis in the WHO region of the Americas: Ecuador’s progress towards verification of elimination. Wkly Epidemiol Rec 89: 401–405.
-
13.
World Health Organization, 2015. Progress toward eliminating onchocerciasis in the WHO region of the Americas: verification of elimination of transmission in Mexico. Wkly Epidemiol Rec 90: 577–581.
-
14.
World Health Organization, 2010. African programme for onchocerciasis control—report of the sixth meeting of National Task Forces, October 2009. Wkly Epidemiol Rec 85: 23–28.
-
15.
World Health Organization, 1995. Onchocerciasis and its control. Report of a WHO expert committee on onchocerciasis control. World Health Organ Tech Rep Ser 852: 1–104.
-
16.
Bottomley C, Isham V, Vivas-Martinez S, Kuesel AC, Attah SK, Opoku NO, Lustigman S, Walker M, Basanez MG, 2016. Modelling neglected tropical diseases diagnostics: the sensitivity of skin snips for Onchocerca volvulus in near elimination and surveillance settings. Parasit Vectors 9: 343.
-
17.
Thiele EA, Cama VA, Lakwo T, Mekasha S, Abanyie F, Sleshi M, Kebede A, Cantey PT, 2016. Detection of Onchocerca volvulus in skin snips by microscopy and real-time polymerase chain reaction: implications for monitoring and evaluation activities. Am J Trop Med Hyg 94: 906–911.
-
18.
Toe L, Boatin BA, Adjami A, Back C, Merriweather A, Unnasch TR, 1998. Detection of Onchocerca volvulus infection by O-150 polymerase chain reaction analysis of skin scratches. J Infect Dis 178: 282–285.
-
19.
Lobos E, Altmann M, Mengod G, Weiss N, Rudin W, Karam M, 1990. Identification of an Onchocerca volvulus cDNA encoding a low-molecular-weight antigen uniquely recognized by onchocerciasis patient sera. Mol Biochem Parasitol 39: 135–145.
-
20.
Lobos E, Weiss N, Karam M, Taylor HR, Ottesen EA, Nutman TB, 1991. An immunogenic Onchocerca volvulus antigen: a specific and early marker of infection. Science 251: 1603–1605.
-
21.
Lazzeri M, Nutman T, Weiss N, 1995. Nucleotide Molecule Enconding a Specific Onchocerca volvulus Antigen for the Immunodiagnosis of onchocerciasis. USPTO, ed. Washington, DC: United Stated Patent and Trademark Office. United States Patent Number: 5,416,009.
-
22.
Ogunrinade AF, Awolola SO, Rotimi O, Chandrashekar R, 2000. Longitudinal studies of skin microfilaria and antibody conversion rates in children living in an endemic focus of onchocerciasis in Nigeria. J Trop Pediatr 46: 348–351.
-
23.
Rodriguez-Perez MA, Unnasch TR, Dominguez-Vazquez A, Morales-Castro AL, Pena-Flores GP, Orozco-Algarra ME, Arredondo-Jimenez JI, Richards F Jr., Vasquez-Rodriguez MA, Rendon VG, 2010. Interruption of transmission of Onchocerca volvulus in the Oaxaca focus, Mexico. Am J Trop Med Hyg 83: 21–27.
-
24.
Zarroug IM et al. 2016. The first confirmed elimination of an onchocerciasis focus in Africa: Abu Hamed, Sudan. Am J Trop Med Hyg 95: 1037–1040.
-
25.
Eberhard ML, Dickerson JW, Boyer AE, Tsang VC, Zea-Flores R, Walker EM, Richards FO, Zea-Flores G, Strobert E, 1991. Experimental Onchocerca volvulus infections in mangabey monkeys (Cercocebus atys) compared to infections in humans and chimpanzees (Pan troglodytes). Am J Trop Med Hyg 44: 151–160.
-
26.
Eberhard ML et al. 1995. Onchocerca volvulus: parasitologic and serologic responses in experimentally infected chimpanzees and mangabey monkeys. Exp Parasitol 80: 454–462.
-
27.
Abraham D, Lange AM, Yutanawiboonchai W, Trpis M, Dickerson JW, Swenson B, Eberhard ML, 1993. Survival and development of larval Onchocerca volvulus in diffusion chambers implanted in primate and rodent hosts. J Parasitol 79: 571–582.
-
28.
Cruz-Ortiz N, Gonzalez RJ, Lindblade KA, Richards FO Jr., Sauerbrey M, Zea-Flores G, Dominguez A, Oliva O, Catu E, Rizzo N, 2012. Elimination of Onchocerca volvulus transmission in the Huehuetenango focus of Guatemala. J Parasitol Res 2012: 638429.
-
29.
Press WH, Flannery BP, Teukolski SA, Vetterling WT, 1988. Numerical Recipes in C: The Art of Scientific Computing. New York, NY: Cambridge University Press.
-
30.
Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, Muller M, 2011. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 12: 77.
-
31.
Burbelo PD, Leahy HP, Iadarola MJ, Nutman TB, 2009. A four-antigen mixture for rapid assessment of Onchocerca volvulus infection. PLoS Negl Trop Dis 3: e438.
-
32.
Golden A et al. 2013. Extended result reading window in lateral flow tests detecting exposure to Onchocerca volvulus: a new technology to improve epidemiological surveillance tools. PLoS One 8: e69231.
-
33.
Gass K, 2018. Rethinking the serological threshold for onchocerciasis elimination. PLoS Negl Trop Dis 12: e0006249.
-
34.
Boyer AE, Tsang VC, Eberhard ML, Zea-Flores G, Hightower A, Pilcher JB, Zea-Flores R, Zhou W, Reimer CB, 1991. Guatemalan human onchocerciasis. II. Evidence for IgG3 involvement in acquired immunity to Onchocerca volvulus and identification of possible immune-associated antigens. J Immunol 146: 4001–4010.
-
35.
Tsang VC, Boyer AE, Pilcher JB, Eberhard ML, Reimer CB, Zea-Flores G, Zea-Flores R, Zhou W, Richards FO, 1991. Guatemalan human onchocerciasis. I. Systematic analysis of patient populations, nodular antigens, and specific isotypic reactions. J Immunol 146: 3993–4000.
-
36.
Weiss N, 1986. Immunological approaches to the detection of prepatent onchocerciasis. J Commun Dis 18: 254–260.
-
37.
Henry NL, Law M, Nutman TB, Klion AD, 2001. Onchocerciasis in a nonendemic population: clinical and immunologic assessment before treatment and at the time of presumed cure. J Infect Dis 183: 512–516.
-
38.
Evans DS et al. 2014. Status of Onchocerciasis transmission after more than a decade of mass drug administration for onchocerciasis and lymphatic filariasis elimination in central Nigeria: challenges in coordinating the stop MDA decision. PLoS Negl Trop Dis 8: e3113.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 3871 | 3300 | 212 |
| Full Text Views | 1146 | 21 | 2 |
| PDF Downloads | 255 | 22 | 0 |