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Journal of Tropical Medicine
Volume 2017, Article ID 7364854, 10 pages
https://doi.org/10.1155/2017/7364854
Research Article

Development and Validation of a PCR-ELISA for the Diagnosis of Symptomatic and Asymptomatic Infection by Leishmania (Leishmania) infantum

1Centro de Pesquisas René Rachou, Oswaldo Cruz Foundation (Fiocruz), Belo Horizonte, MG, Brazil
2Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil

Correspondence should be addressed to Edward Oliveira; rb.zurcoif.rrqpc@ojdrawde

Received 31 August 2016; Accepted 7 December 2016; Published 9 January 2017

Academic Editor: Sukla Biswas

Copyright © 2017 Fernanda Alvarenga Cardoso Medeiros et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. WHO, “Leishmaniasis in high-burden countries: an epidemiological update based on data reported in 2014,” Weekly Epidemiological Record, vol. 22, pp. 287–296, 2016. View at Google Scholar
  2. M. O. Harhay, P. L. Olliaro, D. L. Costa, and C. H. N. Costa, “Urban parasitology: visceral leishmaniasis in Brazil,” Trends in Parasitology, vol. 27, no. 9, pp. 403–409, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. V. E. M. de Araújo, L. C. Pinheiro, M. C. M. de Almeida et al., “Relative risk of visceral leishmaniasis in Brazil: a spatial analysis in urban area,” PLoS Neglected Tropical Diseases, vol. 7, no. 11, article no. e2540, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. SINAN-Sistema de Informação de Agravos de Notificação, Ministério da Saúde, Brasília, 2015, http://datasus.saude.gov.br/.
  5. K. Ritmeijer, Y. Melaku, M. Mueller, S. Kipngetich, C. O'Keeffe, and R. N. Davidson, “Evaluation of a new recombinant K39 rapid diagnostic test for Sudanese visceral leishmaniasis,” American Journal of Tropical Medicine and Hygiene, vol. 74, no. 1, pp. 76–80, 2006. View at Google Scholar · View at Scopus
  6. E. Abass, C. Kang, F. Martinkovic et al., “Heterogeneity of Leishmania donovani parasites complicates diagnosis of visceral leishmaniasis: comparison of different serological tests in three endemic regions,” PLoS ONE, vol. 10, no. 3, Article ID e0116408, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Ter Horst, T. Tefera, G. Assefa, A. Z. Ebrahim, R. N. Davidson, and K. Ritmeijer, “Field evaluation of rK39 test and direct agglutination test for diagnosis of visceral leishmaniasis in a population with high prevalence of human immunodeficiency virus in Ethiopia,” The American Journal of Tropical Medicine and Hygiene, vol. 80, no. 6, pp. 929–934, 2009. View at Google Scholar · View at Scopus
  8. G. F. Cota, M. R. de Sousa, F. N. Demarqui, and A. Rabello, “The diagnostic accuracy of serologic and molecular methods for detecting visceral leishmaniasis in HIV infected patients: meta-analysis,” PLoS Neglected Tropical Diseases, vol. 6, no. 5, Article ID e1665, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. G. F. Cota, M. R. De Sousa, B. M. De Freitas Nogueira et al., “Comparison of parasitological, serological, and molecular tests for visceral leishmaniasis in HIV-infected patients: a cross-sectional delayed-type study,” American Journal of Tropical Medicine and Hygiene, vol. 89, no. 3, pp. 570–577, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Andreadou, E. Liandris, I. N. Kasampalidis et al., “Evaluation of the performance of selected in-house and commercially available PCR and real-time PCR assays for the detection of Leishmania DNA in canine clinical samples,” Experimental Parasitology, vol. 131, no. 4, pp. 419–424, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. G. Srividya, A. Kulshrestha, R. Singh, and P. Salotra, “Diagnosis of visceral leishmaniasis: developments over the last decade,” Parasitology Research, vol. 110, no. 3, pp. 1065–1078, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. A. M. Montalvo, J. Fraga, I. Maes, J.-C. Dujardin, and G. Van Der Auwera, “Three new sensitive and specific heat-shock protein 70 PCRs for global Leishmania species identification,” European Journal of Clinical Microbiology & Infectious Diseases, vol. 31, no. 7, pp. 1453–1461, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. I. S. Koltas, F. Eroglu, S. Uzun, and D. Alabaz, “A comparative analysis of different molecular targets using PCR for diagnosis of old world leishmaniasis,” Experimental Parasitology, vol. 164, pp. 43–48, 2016. View at Publisher · View at Google Scholar
  14. L. Lachaud, S. Marchergui-Hammami, E. ChabbertDereure, J. Dereure, J. P. Dedet, and P. Bastien, “Comparison of six PCR methods using peripheral blood for detection of canine visceral leishmaniasis,” Journal Clinical Microbiology, vol. 40, no. 1, pp. 210–215, 2002. View at Publisher · View at Google Scholar
  15. Z. Wu, Y. Bao, Y. Ding, M. Yu, L. Lu, and Y. Zhang, “An experimental study on application of PCR in detection of Kala-azar,” The Southeast Asian Journal of Tropical Medicine and Public Health, vol. 28, no. 1, pp. 169–172, 1997. View at Google Scholar · View at Scopus
  16. R. Maurya, R. K. Singh, B. Kumar, P. Salotra, M. Rai, and S. Sundar, “Evaluation of PCR for diagnosis of Indian kala-azar and assessment of cure,” Journal of Clinical Microbiology, vol. 43, no. 7, pp. 3038–3041, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Banoo, D. Bell, P. Bossuyt et al., “Evaluation of diagnostic tests for infectious diseases: general principles,” Nature Reviews Microbiology, vol. 4, no. 9, pp. S21–S31, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. Â. C. Volpini, V. M. A. Passos, G. C. Oliveira, and A. J. Romanha, “PCR-RFLP to identify Leishmania (Viannia) braziliensis and L. (Leishmania) amazonensis causing American cutaneous leishmaniasis,” Acta Tropica, vol. 90, no. 1, pp. 31–37, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Rozen and H. Skaletsky, “Primer3 on the WWW for general users and for biologist programmers,” Methods in molecular biology (Clifton, N.J.), vol. 132, pp. 365–386, 2000. View at Google Scholar · View at Scopus
  20. E. Luneberg, J. S. Jensen, and M. Frosch, “Detection of Mycoplasma pneumoniae by polymerase chain reaction and nonradioactive hybridization in microtiter plates,” Journal of Clinical Microbiology, vol. 31, no. 5, pp. 1088–1094, 1993. View at Google Scholar · View at Scopus
  21. L. I. Gomes, L. H. Dos Santos Marques, M. J. Enk, M. C. de Oliveira, P. M. Z. Coelho, and A. Rabello, “Development and evaluation of a sensitive PCR-ELISA system for detection of Schistosoma infection in feces,” PLoS Neglected Tropical Diseases, vol. 4, no. 4, article e664, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. O. Musso, P. Sommer, E. Drouet et al., “In situ detection of human cytomegalovirus DNA in gastrointestinal biopsies from AIDS patients by means of various PCR-derived methods,” Journal of Virological Methods, vol. 56, no. 2, pp. 125–137, 1996. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Antinori, L. Schifanella, and M. Corbellino, “Leishmaniasis: new insights from an old and neglected disease,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 31, no. 2, pp. 109–118, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. M. J. Sue, S. K. Yeap, A. R. Omar, and S. W. Tan, “Application of PCR-ELISA in molecular diagnosis,” BioMed Research International, vol. 2014, Article ID 653014, 6 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. C. M. De Ruiter, C. Van Der Veer, M. M. G. Leeflang, S. Deborggraeve, C. Lucas, and E. R. Adams, “Molecular tools for diagnosis of visceral leishmaniasis: systematic review and meta-analysis of diagnostic test accuracy,” Journal of Clinical Microbiology, vol. 52, no. 9, pp. 3147–3155, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. M. R. Rodgers, S. J. Popper, and D. F. Wirth, “Amplification of kinetoplast DNA as a tool in the detection and diagnosis of Leishmania,” Experimental Parasitology, vol. 71, no. 3, pp. 267–275, 1990. View at Publisher · View at Google Scholar · View at Scopus
  27. W. Degrave, O. Fernandes, D. Campbell, M. Bozza, and U. Lopes, “Use of molecular probes and PCR for detection and typing of Leishmania—a mini-review,” Memorias do Instituto Oswaldo Cruz, vol. 89, no. 3, pp. 463–469, 1994. View at Publisher · View at Google Scholar · View at Scopus
  28. J.-M. Costa, R. Durand, M. Deniau et al., “PCR enzyme-linked immunosorbent assay for diagnosis of leishmaniasis in human immunodeficiency virus-infected patients,” Journal of Clinical Microbiology, vol. 34, no. 7, pp. 1831–1833, 1996. View at Google Scholar · View at Scopus
  29. S. De Doncker, V. Hutse, S. Abdellati et al., “A new PCR-ELISA for diagnosis of visceral leishmaniasis in blood of HIV-negative subjects,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 99, no. 1, pp. 25–31, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Alborzi, B. Pourabbas, F. Shahian, J. Mardaneh, G. R. Pouladfar, and M. Ziyaeyan, “Detection of Leishmania infantum kinetoplast DNA in the whole blood of asymptomatic individuals by PCR-ELISA and comparison with other infection markers in endemic areas, southern Iran,” The American Journal of Tropical Medicine and Hygiene, vol. 79, no. 6, pp. 839–842, 2008. View at Google Scholar · View at Scopus
  31. T. Kobets, J. Badalová, I. Grekov, H. Havelková, M. Svobodová, and M. Lipoldová, “Leishmania parasite detection and quantification using PCR-ELISA,” Nature protocols, vol. 5, no. 6, pp. 1074–1080, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. N. Rolão, S. Cortes, O. R. Rodrigues, and L. Campino, “Quantification of Leishmania infantum parasites in tissue biopsies by real-time polymerase chain reaction and polymerase chain reaction-enzyme-linked immunosorbent assay,” Journal of Parasitology, vol. 90, no. 5, pp. 1150–1154, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Martin-Sanchez, M. C. Lopez-Lopez, C. Acedo-Sanchez, J. J. Castro-Fajardo, J. A. Pineda, and F. Morillas-Marquez, “Diagnosis of infections with Leishmania infantum using PCR-ELISA,” Parasitology, vol. 122, no. 6, pp. 607–615, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Martín-Sánchez, J. A. Pineda, M. Andreu-Lopez et al., “The high sensitivity of a PCR-ELISA in the diagnosis of cutaneous and visceral leishmaniasis caused by Leishmania infantum,” Annals of Tropical Medicine and Parasitology, vol. 96, no. 7, pp. 669–677, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Martín-Sánchez and M. M. Francisco, Kit para diagnóstico específico de las leishmaniosis causadas por ‘Leishmania infantum’ por la técnica de PCR-ELISA, Espanha patente CI- C12Q 1/68, 01 Novmber 2003.
  36. P. Morata, M. I. Queipo-Ortuño, J. M. Reguera, M. A. García-Ordoñez, A. Ana Cárdenas, and J. D. Colmenero, “Development and evaluation of a PCR-enzyme-linked immunosorbent assay for diagnosis of human brucellosis,” Journal of Clinical Microbiology, vol. 41, no. 1, pp. 144–148, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. M. I. Queipo-Ortuño, M. A. García-Ordoñez, R. Gil, J. Rojas, J. D. D. Colmenero, and P. Morata, “PCR-DIG ELISA with biotinylated primers is unsuitable for use in whole blood samples from patients with brucellosis,” Molecular and Cellular Probes, vol. 18, no. 4, pp. 243–250, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Musiani, G. Gallinella, S. Venturoli, and M. Zerbini, “Competitive PCR-ELISA protocols for the quantitative and the standardized detection of viral genomes,” Nature Protocols, vol. 2, no. 10, pp. 2511–2519, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Disch, F. C. Maciel, M. C. de Oliveira, M. Orsini, and A. Rabello, “Detection of circulating Leishmania chagasi DNA for the non-invasive diagnosis of human infection,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 97, no. 4, pp. 391–395, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Piarroux, F. Gambarelli, H. Dumon et al., “Comparison of PCR with direct examination of bone marrow aspiration, myeloculture, and serology for diagnosis of visceral leishmaniasis in immunocompromised patients,” Journal of Clinical Microbiology, vol. 32, no. 3, pp. 746–749, 1994. View at Google Scholar · View at Scopus
  41. L. Lachaud, J. Dereure, E. Chabbert et al., “Optimized PCR using patient blood samples for diagnosis and follow-up of visceral leishmaniasis, with special reference to AIDS patients,” Journal of Clinical Microbiology, vol. 38, no. 1, pp. 236–240, 2000. View at Google Scholar · View at Scopus
  42. C. Fissore, P. Delaunay, B. Ferrua et al., “Convenience of serum for visceral leishmaniasis diagnosis by PCR,” Journal of Clinical Microbiology, vol. 42, no. 11, pp. 5332–5333, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. R. F. S. Braz, E. T. Nascimento, D. R. A. Martins et al., “The sensitivity and specificity of Leishmania chagasi recombinant K39 antigen in the diagnosis of American visceral leishmaniasis and in differentiating active from subclinical infection,” American Journal of Tropical Medicine and Hygiene, vol. 67, no. 4, pp. 344–348, 2002. View at Google Scholar · View at Scopus
  44. S. F. Guimarães Carvalho, E. Moreira Lemos, R. Corey, and R. Dietze, “Performance of recombinant K39 antigen in the diagnosis of Brazilian visceral leishmaniasis,” American Journal of Tropical Medicine and Hygiene, vol. 68, no. 3, pp. 321–324, 2003. View at Google Scholar · View at Scopus
  45. M. Boelaert, S. Rijal, S. Regmi et al., “A comparative study of the effectiveness of diagnostic tests for visceral leishmaniasis,” American Journal of Tropical Medicine and Hygiene, vol. 70, no. 1, pp. 72–77, 2004. View at Google Scholar · View at Scopus
  46. F. Chappuis, S. Rijal, A. Soto, J. Menten, and M. Boelaert, “A meta-analysis of the diagnostic performance of the direct agglutination test and rK39 dipstick for visceral leishmaniasis,” British Medical Journal, vol. 333, no. 7571, pp. 723–726, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. Z. Maia, M. Lírio, S. Mistro, C. M. C. Mendes, S. R. Mehta, and R. Badaro, “Comparative study of rK39 Leishmania antigen for serodiagnosis of visceral leishmaniasis: systematic review with meta-analysis,” PLoS Neglected Tropical Diseases, vol. 6, no. 1, Article ID e1484, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. L. de Gouvêa Viana, T. S. M. de Assis, M. Orsini et al., “Combined diagnostic methods identify a remarkable proportion of asymptomatic Leishmania (Leishmania) chagasi carriers who present modulated cytokine profiles,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 102, no. 6, pp. 548–555, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. E. C. Moreno, A. V. Gonçalves, A. V. Chaves et al., “Inaccuracy of enzyme-linked immunosorbent assay using soluble and recombinant antigens to detect asymptomatic infection by Leishmania infantum,” PLoS Neglected Tropical Diseases, vol. 3, no. 10, article no. e536, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. L. H. dos Santos Marques, L. I. Gomes, I. C. M. da Rocha et al., “Low parasite load estimated by qPCR in a cohort of children living in urban area endemic for visceral leishmaniasis in Brazil,” PLoS Neglected Tropical Diseases, vol. 6, no. 12, Article ID e1955, 2012. View at Publisher · View at Google Scholar · View at Scopus