ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2011. African programme for onchocerciasis control: meeting of National Task Forces, September, 2011. Wkly Epidemiol Rec 86: 541–549.
-
2.
Richards FO, Miri E, Meredith S, Guderian R, Sauerbrey M, Remme H, Packard R, Ndiaye JM, 1998. Onchocerciasis. Bull World Health Organ 76: 147–149.
-
3.
Roberts JMD, Neumann E, Göckel CW, Highton RB, 1967. Onchocerciasis in Kenya 9, 11 and 18 years after elimination of the vector. Bull World Health Organ 37: 195–212.
-
4.
Turner HC, Walker M, Churcher TS, Basáñez MG, 2014. Modelling the impact of ivermectin on River Blindness and its burden of morbidity and mortality in African Savannah: EpiOncho projections. Parasit Vectors 7: 241.
-
5.
World Health Organization, 2001. Criteria for Certification of Interruption of Transmission/Elimination of Human Onchocerciasis. Document WHO/CDS/CEE/2001.18a. Geneva, Switzerland: WHO.
-
6.
Lindblade KA, Arana B, Zea-Flores G, Rizzo N, Porter CH, Dominguez A, Cruz-Ortiz N, Unnasch TR, Punkosdy GA, Richards J, Sauerbrey M, Castro J, Catú E, Oliva O, Richards FO Jr, 2007. Elimination of Onchocercia volvulus transmission in the Santa Rosa focus of Guatemala. Am J Trop Med Hyg 77: 334–341.
-
7.
Diawara L, Traoré MO, Badji A, Bissan Y, Doumbia K, Goita SF, Konaté L, Mounkoro K, Sarr MD, Seck AF, Toé L, Tourée S, Remme JH, 2009. Feasibility of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: first evidence from studies in Mali and Senegal. PLoS Negl Trop Dis 3: e497.
-
8.
Taylor HR, Munoz B, Keyvan-Larijani E, Greene BM, 1989. Reliability of detection of microfilariae in skin snips in the diagnosis of onchocerciasis. Am J Trop Med Hyg 41: 467–471.
-
9.
Basáñez M-G, Pion SDS, Boakes E, Filipe JAN, Churcher TS, Boussinesq M, 2008. Effect of single-dose ivermectin on Onchocerca volvulus: a systematic review and meta-analysis. Lancet Infect Dis 8: 310–322.
-
10.
Boatin BA, Toe L, Alley ES, Nagelkerke NJ, Borsboom G, Habbema JD, 2002. Detection of Onchocerca volvulus infection in low prevalence areas: a comparison of three diagnostic methods. Parasitology 125: 545–552.
-
11.
Morales-Hojas R, Post RJ, Shelley AJ, Maia-Herzog M, Coscaron S, Cheke RA, 2001. Characterisation of nuclear ribosomal DNA sequences from Onchocerca volvulus and Mansonella ozzardi (Nematoda: Filarioidea) and development of a PCR-based method for their detection in skin biopsies. Int J Parasitol 31: 169–177.
-
12.
Rishniw M, Barr SC, Simpson KW, Frongillo MF, Franz M, Dominguez Alpizar JL, 2006. Discrimination between six species of canine microfilariae by a single polymerase chain reaction. Vet Parasitol 135: 303–314.
-
13.
Tang TH, Lopez-Velez R, Lanza M, Shelley AJ, Rubio JM, Luz SL, 2010. Nested PCR to detect and distinguish the sympatric filarial species Onchocerca volvulus, Mansonella ozzardi and Mansonella perstans in the Amazon Region. Mem Inst Oswaldo Cruz 105: 823–828.
-
14.
Collins RC, Brandling-Bennett AD, Holliman RB, Campbell CC, Darsie RF, 1980. Parasitological diagnosis of onchocerciasis: comparisons of incubation media and incubation times for skin snips. Am J Trop Med Hyg 29: 35–41.
-
15.
Unnasch TR, Meredith SE, 1996. The use of degenerate primers in conjunction with strain and species oligonucleotides to classify Onchocerca volvulus. Clapp JP, ed. Methods in Molecular Biology, Vol. 50. Totowa, NJ: Humana Press Inc., 293–303.
-
16.
Fink DL, Fahle GA, Fischer S, Fedorko DF, Nutman TB, 2011. Toward molecular parasitologic diagnosis: enhanced diagnostic sensitivity for filarial infections in mobile populations. J Clin Microbiol 49: 42–47.
-
17.
Lloyd MM, Gilbert R, Taha NT, Weil GJ, Meite A, Kouakou IMM, Fischer PU, 2015. Conventional parasitology and DNA-based diagnostic methods for onchocerciasis elimination programmes. Acta Trop 146: 114–118.
-
18.
Fischer P, Buttner DW, Bamuhiiga J, Williams SA, 1998. Detection of the filarial parasite Mansonella streptocerca in skin biopsies by a nested polymerase chain reaction-based assay. Am J Trop Med Hyg 58: 816–820.
-
19.
Nuchprayoon S, Junpee A, Poovorawan Y, Scott AL, 2005. Detection and differentiation of filarial parasites by universal primers and polymerase chain reaction-restriction fragment length polymorphism analysis. Am J Trop Med Hyg 73: 895–900.
-
20.
Jiménez M, González LM, Carranza C, Bailo B, Pérez-Ayala A, Muro A, Pérez-Arellano JL, Gárate T, 2011. Detection and discrimination of Loa loa, Mansonella perstans and Wuchereria bancrofti by PCR-RFLP and nested-PCR of ribosomal DNA ITS1 region. Exp Parasitol 127: 282–286.
-
21.
Poole CB, Tanner NA, Zhang Y, Evans TC Jr, Carlow CK, 2012. Diagnosis of brugian filariasis by loop-mediated isothermal amplification. PLoS Negl Trop Dis 6: e1948.
-
22.
Gopal H, Hassan HK, Rodriguez-Perez MA, Toe LD, Lustigman S, Unnasch TR, 2012. Oligonucleotide based magnetic bead capture of Onchocerca volvulus DNA for PCR pool screening of vector black flies. PLoS Negl Trop Dis 6: e1712.
-
23.
Pilotte N, Torres M, Tomaino FR, Laney SJ, Williams SA, 2013. A TaqMan-based multiplex real-time PCR assay for the simultaneous detection of Wuchereria bancrofti and Brugia malayi. Mol Biochem Parasitol 189: 33–37.
-
24.
Zimmerman PA, Guderian RH, Aruajo E, Elson L, Phadke P, Kubofcik J, Nutman TB, 1994. Polymerase chain reaction-based diagnosis of Onchocerca volvulus infection: improved detection of patients with onchocerciasis. J Infect Dis 169: 686–689.
-
25.
Toé 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.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 920 | 729 | 47 |
| Full Text Views | 863 | 11 | 0 |
| PDF Downloads | 334 | 12 | 0 |
Detection of Onchocerca volvulus in Skin Snips by Microscopy and Real-Time Polymerase Chain Reaction: Implications for Monitoring and Evaluation Activities
Elizabeth A. Thiele
Elizabeth A. Thiele
Parasitic Diseases Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee; Vector Control Division, Ministry of Health, Kampala, Uganda; Ethiopian Public Health Institute, Addis Ababa, Ethiopia
Search for other papers by Elizabeth A. Thiele in
Current site
Google Scholar
PubMed
Search for other papers by Elizabeth A. Thiele in
Current site
Google Scholar
PubMed
Vitaliano A. Cama
Vitaliano A. Cama
Parasitic Diseases Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee; Vector Control Division, Ministry of Health, Kampala, Uganda; Ethiopian Public Health Institute, Addis Ababa, Ethiopia
Search for other papers by Vitaliano A. Cama in
Current site
Google Scholar
PubMed
Search for other papers by Vitaliano A. Cama in
Current site
Google Scholar
PubMed
Thomson Lakwo
Thomson Lakwo
Parasitic Diseases Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee; Vector Control Division, Ministry of Health, Kampala, Uganda; Ethiopian Public Health Institute, Addis Ababa, Ethiopia
Search for other papers by Thomson Lakwo in
Current site
Google Scholar
PubMed
Search for other papers by Thomson Lakwo in
Current site
Google Scholar
PubMed
Sindeaw Mekasha
Sindeaw Mekasha
Parasitic Diseases Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee; Vector Control Division, Ministry of Health, Kampala, Uganda; Ethiopian Public Health Institute, Addis Ababa, Ethiopia
Search for other papers by Sindeaw Mekasha in
Current site
Google Scholar
PubMed
Search for other papers by Sindeaw Mekasha in
Current site
Google Scholar
PubMed
Francisca Abanyie
Francisca Abanyie
Parasitic Diseases Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee; Vector Control Division, Ministry of Health, Kampala, Uganda; Ethiopian Public Health Institute, Addis Ababa, Ethiopia
Search for other papers by Francisca Abanyie in
Current site
Google Scholar
PubMed
Search for other papers by Francisca Abanyie in
Current site
Google Scholar
PubMed
Markos Sleshi
Markos Sleshi
Parasitic Diseases Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee; Vector Control Division, Ministry of Health, Kampala, Uganda; Ethiopian Public Health Institute, Addis Ababa, Ethiopia
Search for other papers by Markos Sleshi in
Current site
Google Scholar
PubMed
Search for other papers by Markos Sleshi in
Current site
Google Scholar
PubMed
Amha Kebede
Amha Kebede
Parasitic Diseases Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee; Vector Control Division, Ministry of Health, Kampala, Uganda; Ethiopian Public Health Institute, Addis Ababa, Ethiopia
Search for other papers by Amha Kebede in
Current site
Google Scholar
PubMed
Search for other papers by Amha Kebede in
Current site
Google Scholar
PubMed
Paul T. Cantey
Paul T. Cantey
Parasitic Diseases Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Oak Ridge Institute for Science and Education, Oak Ridge, Tennessee; Vector Control Division, Ministry of Health, Kampala, Uganda; Ethiopian Public Health Institute, Addis Ababa, Ethiopia
Search for other papers by Paul T. Cantey in
Current site
Google Scholar
PubMed
Search for other papers by Paul T. Cantey in
Current site
Google Scholar
PubMed
Microscopic evaluation of skin biopsies is the monitoring and evaluation (M and E) method currently used by multiple onchocerciasis elimination programs in Africa. However, as repeated mass drug administration suppresses microfilarial loads, the sensitivity and programmatic utility of skin snip microscopy is expected to decrease. Using a pan-filarial real-time polymerase chain reaction with melt curve analysis (qPCR-MCA), we evaluated 1) the use of a single-step molecular assay for detecting and identifying Onchocerca volvulus microfilariae in residual skin snips and 2) the sensitivity of skin snip microscopy relative to qPCR-MCA. Skin snips were collected and examined with routine microscopy in hyperendemic regions of Uganda and Ethiopia (N = 500 each) and “residual” skin snips (tissue remaining after induced microfilarial emergence) were tested with qPCR-MCA. qPCR-MCA detected Onchocerca DNA in 223 residual snips: 139 of 147 microscopy(+) and 84 among microscopy(−) snips, suggesting overall sensitivity of microscopy was 62.3% (139/223) relative to qPCR-MCA (75.6% in Uganda and 28.6% in Ethiopia). These findings demonstrate the insufficient sensitivity of skin snip microscopy for reliable programmatic monitoring. Molecular tools such as qPCR-MCA can augment sensitivity and provide diagnostic confirmation of skin biopsies and will be useful for evaluation or validation of new onchocerciasis M and E tools.
Author Notes
Financial support: This work was supported by a grant from the Bill & Melinda Gates Foundation. Elizabeth A. Thiele was supported by a Postdoctoral Fellowship through the Oak Ridge Institute for Science and Education (ORISE).
Authors' addresses: Elizabeth A. Thiele, Department of Biology, Vassar College, Poughkeepsie, NY, E-mail: elthiele@vassar.edu. Vitaliano A. Cama, Francisca Abanyie, and Paul T. Cantey, Parasitic Diseases Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: vcama@cdc.gov, why6@cdc.gov, and pcantey@cdc.gov. Thomson Lakwo, Vector Control Division, Ministry of Health, Kampala, Uganda, E-mail: tlakwo@gmail.com. Sindeaw Mekasha, Markos Sleshi, and Amha Kebede, Ethiopian Public Health Institute, Addis Ababa, Ethiopia, E-mails: mekashasindeaw@yahoo.com, markossleshi@yahoo.com, and amha.kebede@gmail.com.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2011. African programme for onchocerciasis control: meeting of National Task Forces, September, 2011. Wkly Epidemiol Rec 86: 541–549.
-
2.
Richards FO, Miri E, Meredith S, Guderian R, Sauerbrey M, Remme H, Packard R, Ndiaye JM, 1998. Onchocerciasis. Bull World Health Organ 76: 147–149.
-
3.
Roberts JMD, Neumann E, Göckel CW, Highton RB, 1967. Onchocerciasis in Kenya 9, 11 and 18 years after elimination of the vector. Bull World Health Organ 37: 195–212.
-
4.
Turner HC, Walker M, Churcher TS, Basáñez MG, 2014. Modelling the impact of ivermectin on River Blindness and its burden of morbidity and mortality in African Savannah: EpiOncho projections. Parasit Vectors 7: 241.
-
5.
World Health Organization, 2001. Criteria for Certification of Interruption of Transmission/Elimination of Human Onchocerciasis. Document WHO/CDS/CEE/2001.18a. Geneva, Switzerland: WHO.
-
6.
Lindblade KA, Arana B, Zea-Flores G, Rizzo N, Porter CH, Dominguez A, Cruz-Ortiz N, Unnasch TR, Punkosdy GA, Richards J, Sauerbrey M, Castro J, Catú E, Oliva O, Richards FO Jr, 2007. Elimination of Onchocercia volvulus transmission in the Santa Rosa focus of Guatemala. Am J Trop Med Hyg 77: 334–341.
-
7.
Diawara L, Traoré MO, Badji A, Bissan Y, Doumbia K, Goita SF, Konaté L, Mounkoro K, Sarr MD, Seck AF, Toé L, Tourée S, Remme JH, 2009. Feasibility of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: first evidence from studies in Mali and Senegal. PLoS Negl Trop Dis 3: e497.
-
8.
Taylor HR, Munoz B, Keyvan-Larijani E, Greene BM, 1989. Reliability of detection of microfilariae in skin snips in the diagnosis of onchocerciasis. Am J Trop Med Hyg 41: 467–471.
-
9.
Basáñez M-G, Pion SDS, Boakes E, Filipe JAN, Churcher TS, Boussinesq M, 2008. Effect of single-dose ivermectin on Onchocerca volvulus: a systematic review and meta-analysis. Lancet Infect Dis 8: 310–322.
-
10.
Boatin BA, Toe L, Alley ES, Nagelkerke NJ, Borsboom G, Habbema JD, 2002. Detection of Onchocerca volvulus infection in low prevalence areas: a comparison of three diagnostic methods. Parasitology 125: 545–552.
-
11.
Morales-Hojas R, Post RJ, Shelley AJ, Maia-Herzog M, Coscaron S, Cheke RA, 2001. Characterisation of nuclear ribosomal DNA sequences from Onchocerca volvulus and Mansonella ozzardi (Nematoda: Filarioidea) and development of a PCR-based method for their detection in skin biopsies. Int J Parasitol 31: 169–177.
-
12.
Rishniw M, Barr SC, Simpson KW, Frongillo MF, Franz M, Dominguez Alpizar JL, 2006. Discrimination between six species of canine microfilariae by a single polymerase chain reaction. Vet Parasitol 135: 303–314.
-
13.
Tang TH, Lopez-Velez R, Lanza M, Shelley AJ, Rubio JM, Luz SL, 2010. Nested PCR to detect and distinguish the sympatric filarial species Onchocerca volvulus, Mansonella ozzardi and Mansonella perstans in the Amazon Region. Mem Inst Oswaldo Cruz 105: 823–828.
-
14.
Collins RC, Brandling-Bennett AD, Holliman RB, Campbell CC, Darsie RF, 1980. Parasitological diagnosis of onchocerciasis: comparisons of incubation media and incubation times for skin snips. Am J Trop Med Hyg 29: 35–41.
-
15.
Unnasch TR, Meredith SE, 1996. The use of degenerate primers in conjunction with strain and species oligonucleotides to classify Onchocerca volvulus. Clapp JP, ed. Methods in Molecular Biology, Vol. 50. Totowa, NJ: Humana Press Inc., 293–303.
-
16.
Fink DL, Fahle GA, Fischer S, Fedorko DF, Nutman TB, 2011. Toward molecular parasitologic diagnosis: enhanced diagnostic sensitivity for filarial infections in mobile populations. J Clin Microbiol 49: 42–47.
-
17.
Lloyd MM, Gilbert R, Taha NT, Weil GJ, Meite A, Kouakou IMM, Fischer PU, 2015. Conventional parasitology and DNA-based diagnostic methods for onchocerciasis elimination programmes. Acta Trop 146: 114–118.
-
18.
Fischer P, Buttner DW, Bamuhiiga J, Williams SA, 1998. Detection of the filarial parasite Mansonella streptocerca in skin biopsies by a nested polymerase chain reaction-based assay. Am J Trop Med Hyg 58: 816–820.
-
19.
Nuchprayoon S, Junpee A, Poovorawan Y, Scott AL, 2005. Detection and differentiation of filarial parasites by universal primers and polymerase chain reaction-restriction fragment length polymorphism analysis. Am J Trop Med Hyg 73: 895–900.
-
20.
Jiménez M, González LM, Carranza C, Bailo B, Pérez-Ayala A, Muro A, Pérez-Arellano JL, Gárate T, 2011. Detection and discrimination of Loa loa, Mansonella perstans and Wuchereria bancrofti by PCR-RFLP and nested-PCR of ribosomal DNA ITS1 region. Exp Parasitol 127: 282–286.
-
21.
Poole CB, Tanner NA, Zhang Y, Evans TC Jr, Carlow CK, 2012. Diagnosis of brugian filariasis by loop-mediated isothermal amplification. PLoS Negl Trop Dis 6: e1948.
-
22.
Gopal H, Hassan HK, Rodriguez-Perez MA, Toe LD, Lustigman S, Unnasch TR, 2012. Oligonucleotide based magnetic bead capture of Onchocerca volvulus DNA for PCR pool screening of vector black flies. PLoS Negl Trop Dis 6: e1712.
-
23.
Pilotte N, Torres M, Tomaino FR, Laney SJ, Williams SA, 2013. A TaqMan-based multiplex real-time PCR assay for the simultaneous detection of Wuchereria bancrofti and Brugia malayi. Mol Biochem Parasitol 189: 33–37.
-
24.
Zimmerman PA, Guderian RH, Aruajo E, Elson L, Phadke P, Kubofcik J, Nutman TB, 1994. Polymerase chain reaction-based diagnosis of Onchocerca volvulus infection: improved detection of patients with onchocerciasis. J Infect Dis 169: 686–689.
-
25.
Toé 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.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 920 | 729 | 47 |
| Full Text Views | 863 | 11 | 0 |
| PDF Downloads | 334 | 12 | 0 |