The direct agglutination test as an alternative method for the diagnosis of canine and human visceral leishmaniasis
Keywords:
Leishmaniasis, visceral/diagnosis, agglutination tests, Leishmania donovani, humans, dogs, Venezuela
Abstract
Introduction. Visceral leishmaniasis is the most severe clinical form of leishmaniasis and is often fatal without proper treatment. Therefore, early and accurate diagnosis is important, butoften difficult in endemic areas.
Objective. The aim was to evaluate a direct agglutination test as a potential visceral leishmaniasis diagnostic method in endemic areas of Venezuela.
Materials and methods. The performance of the direct agglutination test, based on freezedried Leishmania donovani antigen was evaluated under laboratory conditions using serum samples of humans and dogs from several Venezuelan visceral leishmaniasis endemic areas: Nueva Esparta (Margarita Island), Lara, Anzoátegui and Trujillo Status. The study included confirmed visceral leishmaniasis patients (n=30), visceral leishmaniasis suspected subjects (n=4), healthy controls (n=19) and patients with other confirmed diseases (n=20). In addition, 24 serum samples from dogs with confirmed visceral leishmaniasis and 18 healthy control dogs were tested.
Results. All serum samples of visceral leishmaniasis patients, either active or recovered, were positive. They showed anti-L. donovani titers above 1:1600. Three out of four suspected visceral leishmaniasis cases were also positive, while serum samples from endemic controls and patients with other diseases had titers lower than 1:800. A sensitivity of 100% was obtained for all threshold levels under consideration and 100% specificity at the threshold titer of 1:800 (95% confidence interval: 91-100%). A 93% sensitivity (95% confidence interval: 76-99%) was observed in dog samples, with 100% specificity (95% confidence interval: 79-100%) at the threshold titer of 1:200.
Conclusion. The direct agglutination test seems suitable for use in epidemiological studies and for serological diagnosis of human visceral leishmaniasis and canine visceral leishmaniasis.
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References
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4. MSDS-Ministerio de Salud y Desarrollo Social 2004. Leishmaniasis visceral en Venezuela. Caracas: Departamento de Informática, Instituto de Biomedicina; 2003.
5. Zerpa O, Ulrich M, Benitez M, Avila C, Rodriguez V, Centeno M et al. Epidemiological and immunological aspects of human visceral leishmaniasis on Margarita Island, Venezuela. Mem Inst Oswaldo Cruz. 2002;97:1079-83.
6. Zerpa O, Ulrich M, Negrón E, Rodríguez N, Centeno M, Rodríguez V, et al. Canine visceral leishmaniasis on Margarita Island (Nueva Esparta, Venezuela). Trans R Soc Trop Med Hyg. 2000;94:484-7.
7. Organización Mundial de la Salud. Manual de la lucha contra la leishmaniasis visceral. Ginebra: OMS; 1996. [Consultado: 14 de marzo de 2007]. Disponible en: htpp:/
www.paho.org/spanish/AD/DPC/CD/Leishmaniasismanual-0.pdf
8. Duxbury RE, Sadun EH. Fluorescent antibody test for the diagnosis of visceral leishmaniasis. Am J Trop Med Hyg. 1964;13:525-9.
9. Badaro R, Reed SG, Carvalho EM. Immunofluorescent antibody test in American cutaneous leishmaniasis: sensitivity and specificity of different morphological form of two Leishmania species. Am J Trop Med Hyg. 1983;32:480-4.
10. Hommel M, Peters W, Ranque J, Quilici M, Lanotte G. The micro-ELISA technique in the serodiagnosis of visceral leishmaniasis. Ann Trop Med Parasitol. 1978;72:213-8.
11. Anthony RL, Christensen HA, Johnson CM. Micro enzyme-linked immunoassay (ELISA) for the diagnosis of New World leishmaniasis. Am J Trop Med Hyg. 1980;29:190-4.
12. Singh S, Gilman-Sachs A, Chang KP, Reed SG. Diagnostic and prognostic value of k39 recombinant antigen in Indian leishmaniasis. J Parasitol. 1995;81:1000-3.
13. Jelinek T, Eichenlaub S, Loscher T. Sensitivity and specificity of a rapid immunochromatographic test for diagnosis of visceral leishmaniasis. Eur J Clin Microbiol Infect Dis. 1999;18:669-70.
14. Oskam L, Nieuwenhuijs JL, Hailu A. Evaluation of the direct agglutination test (DAT) using freeze-dried antigen for the detection of anti-Leishmania antibodies in stored sera from various patient groups in Ethiopia. Trans R Soc Trop Med Hyg. 1999;93:275-7.
15. Schallig HD, Canto-Cavalheiro M, da Silva ES. Evaluation of the direct agglutination test and the rK39 dipstick test for the serodiagnosis of visceral leishmaniasis. Mem Inst Oswaldo Cruz. 2002;97:1015-8.
16. Zijlstra EE, Osman OF, Hofland HW, Oskam L, Ghalib HW, El-Hassan AM, et al. The direct agglutination test for diagnosis of visceral leishmaniasis under field conditions in Sudan: comparison of aqueous and freeze-dried antigens. Trans R Soc Trop Med Hyg. 1997;91:671-3.
17. Boelaert M, El-Safi S, Jacquet D, de Muynck A, van der Stuyft P, Le Ray D. Operational validation of the direct agglutination test for diagnosis of visceral leishmaniasis. Am J Trop Med Hyg. 1999;60:129-34.
18. Boelaert M, El-Safi S, Mousa H, Githure J, Mbati PA, Gurubacharya V, et al. Multi-centre evaluation of repeatability and reproducibility of the direct agglutination test for visceral leishmaniasis. Trop Med Int Health. 1999;4:31-7.
19. Schallig HD, Schoone GJ, Kroon CC, Hailu A, Chappuis F, Veeken H. Development and application of simple diagnostic tools for visceral leishmaniasis. Med Microbiol Immunol. 2001;190:69-71.
20. El Harith A, Kolk AH, Leeuwenburg J, Muigai R, Huigen E, Jelsma T, et al. Improvement of a direct agglutination test for field studies of visceral leishmaniasis. J Clin Microbiol. 1988;26:1321-5.
21. Meredith SE, Kroon NC, Sondorp E, Seaman J, Goris MG, van Ingen CW, et al. Leish kit, a stable direct agglutination test based on freeze-dried antigen for the serodiagnosis of visceral leishmaniasis. J Clin Microbiol .1995;33:1742-5.
22. Altman DG. Practical statistics for medical research. London: Chapman & Hall/CRC Press; 1991.
23. Bimar S, Das VN, Sinha PK, Verma N, Ranjan A, Singh SK, et al. Usefulness of the direct agglutination test in the early detection of subclinical Leishmania donovani infection:a community-based study. Ann Trop Med Parasitol. 2005;99:743-9.
24. Silva ES, Schoone GJ, Gontijo CM, Brazil RP, Pacheco RS, Schallig DF. Application of direct agglutination test (DAT) and fast agglutination screening test (FAST) for sero-diagnosis of visceral leishmaniasis in endemic area of Minas Gerais, Brazil. Kinetoplastid Bio Dis. 2005;4:4.
25. Hailu A. Pre and post-treatment antibody levels in visceral leishmaniasis. Trans R Soc Trop Med Hyg. 1990;84: 673-5.
26. Ponce C, Ponce E, Morrison A, Cruz A, Kreutzer R, MacMahon-Pratt D, et al. Leishmania donovani chagasi: new clinical variant of cutaneous leishmaniasis in Honduras. Lancet. 1991;337:67-70.
27. Stark D, Pett S, Marrito D, Harkness J. Post-kalaazar dermal leishmaniasis due to Leishmania infantum in a human immunodeficiency virus type 1-infected patient. J Clin Microbiol. 2006;44:1178-80.
28. Vasconcelos AB, Sousa AQ, Vasconcelos AW, Diogenes MJ, Mohen H, Grimaldi G Jr, et al. Parisitisme cutan par Leishmania (Leishmania) chagasi au cours de la leishmaniose viscrale Sud-Americaine.
Bull Soc Pathol Exot. 1993;86:101-5.
29. Convit, J, Ulrich M, Fernández CT, Tapia FJ, Cáceres-Dittmar G, Castés M, et al. The clinical and immunological spectrum of American cutaneous leishmaniasis. Trans R Soc Trop Med Hyg. 1993;87:444-8.
30. Gradoni L. Epizootiology of canine leishmaniasis in southern Europe. In: Killick Kendrick R, editor. Canine leishmaniasis an update. Wiesbaden: Hoeschst Roussel Vet; 1999. p.32-9.
31. Askford RW. Leishmaniasis reservoirs and their significance in control. Clin Dermatol. 1996;14:523-32.
32. Courtenay O, Quinnell RJ, Garcez LM, Shaw JJ, Dye C. Infectiousness in a cohort of Brazilian dogs: why culling fails to control visceral leishmaniasis in areas of high transmission. J Infect Dis. 2002;186:1314-20
33. Dantas-Torres F, Brandao-Filho SP. Visceral leishmaniasis in Brazil: revisiting paradigms of epidemiology and control. Rev Inst Med Trop Sao Paulo. 2006;48:151-6.
34. Cardoso L, Schallig HD, Neto F, Kroon N, Rodrigues M. Serological survey of Leishmania infection in dog from the municipality of Peso da Regua (Alto Douro, Portugal) using direct agglutination test (DAT) and fast agglutination test (FAST). Acta Trop. 2004;91:95-100.
35. Da Silva ES, van der Meide WF, Schoone GJ, Gontijo CM, Schallig HD, Brazil RP. Diagnosis of canine leishmaniasis in the endemic area of Belo Horizonte, Minas Gerais, Brazil by parasite, antibody and DNA detection assays. Vet Res Commun. 2006;30:637-43.
36. Neogy AB, Vouldoukis I, Silva OA, Tselentis Y, Lascombe JC, Segalen T, et al. Serodiagnosis and screening of canine visceral Leishmaniasis in an endemic area of Corsica: applicability of a direct agglutination test and immunoblot analysis. Am J Trop Med Hyg. 1992;47:772-7.
37. Oskam L, Slappendel RL, Beijer EG, Kroon NC, van Ingen CW, Ozensoy S, et al. Dog-DAT: a direct agglutination test using stabilized, freeze-dried antigen for the serodiagnosis of canine visceral leishmaniasis. FEMS Immunol Med Microbiol. 1996;16:235-9.
38. Garcez LM, Shaw JJ, Silveira FT. Direct agglutination test in the serodiagnosis of visceral leishmaniasis in the state of Para. Rev Soc Bras Med. 1996;29:165-80.
2. Desjeux P. Leishmaniasis: current situation and new perspectives. Com Immunol Microbiol Infect Dis. 2004;27:305-18.
3. Grimaldi G Jr, Tesh RB, McMahon-Pratt D. A review of the geographic distribution and epidemiology of leishmaniasis in the New World. Am J Trop Med Hyg. 1989;41:687-725.
4. MSDS-Ministerio de Salud y Desarrollo Social 2004. Leishmaniasis visceral en Venezuela. Caracas: Departamento de Informática, Instituto de Biomedicina; 2003.
5. Zerpa O, Ulrich M, Benitez M, Avila C, Rodriguez V, Centeno M et al. Epidemiological and immunological aspects of human visceral leishmaniasis on Margarita Island, Venezuela. Mem Inst Oswaldo Cruz. 2002;97:1079-83.
6. Zerpa O, Ulrich M, Negrón E, Rodríguez N, Centeno M, Rodríguez V, et al. Canine visceral leishmaniasis on Margarita Island (Nueva Esparta, Venezuela). Trans R Soc Trop Med Hyg. 2000;94:484-7.
7. Organización Mundial de la Salud. Manual de la lucha contra la leishmaniasis visceral. Ginebra: OMS; 1996. [Consultado: 14 de marzo de 2007]. Disponible en: htpp:/
www.paho.org/spanish/AD/DPC/CD/Leishmaniasismanual-0.pdf
8. Duxbury RE, Sadun EH. Fluorescent antibody test for the diagnosis of visceral leishmaniasis. Am J Trop Med Hyg. 1964;13:525-9.
9. Badaro R, Reed SG, Carvalho EM. Immunofluorescent antibody test in American cutaneous leishmaniasis: sensitivity and specificity of different morphological form of two Leishmania species. Am J Trop Med Hyg. 1983;32:480-4.
10. Hommel M, Peters W, Ranque J, Quilici M, Lanotte G. The micro-ELISA technique in the serodiagnosis of visceral leishmaniasis. Ann Trop Med Parasitol. 1978;72:213-8.
11. Anthony RL, Christensen HA, Johnson CM. Micro enzyme-linked immunoassay (ELISA) for the diagnosis of New World leishmaniasis. Am J Trop Med Hyg. 1980;29:190-4.
12. Singh S, Gilman-Sachs A, Chang KP, Reed SG. Diagnostic and prognostic value of k39 recombinant antigen in Indian leishmaniasis. J Parasitol. 1995;81:1000-3.
13. Jelinek T, Eichenlaub S, Loscher T. Sensitivity and specificity of a rapid immunochromatographic test for diagnosis of visceral leishmaniasis. Eur J Clin Microbiol Infect Dis. 1999;18:669-70.
14. Oskam L, Nieuwenhuijs JL, Hailu A. Evaluation of the direct agglutination test (DAT) using freeze-dried antigen for the detection of anti-Leishmania antibodies in stored sera from various patient groups in Ethiopia. Trans R Soc Trop Med Hyg. 1999;93:275-7.
15. Schallig HD, Canto-Cavalheiro M, da Silva ES. Evaluation of the direct agglutination test and the rK39 dipstick test for the serodiagnosis of visceral leishmaniasis. Mem Inst Oswaldo Cruz. 2002;97:1015-8.
16. Zijlstra EE, Osman OF, Hofland HW, Oskam L, Ghalib HW, El-Hassan AM, et al. The direct agglutination test for diagnosis of visceral leishmaniasis under field conditions in Sudan: comparison of aqueous and freeze-dried antigens. Trans R Soc Trop Med Hyg. 1997;91:671-3.
17. Boelaert M, El-Safi S, Jacquet D, de Muynck A, van der Stuyft P, Le Ray D. Operational validation of the direct agglutination test for diagnosis of visceral leishmaniasis. Am J Trop Med Hyg. 1999;60:129-34.
18. Boelaert M, El-Safi S, Mousa H, Githure J, Mbati PA, Gurubacharya V, et al. Multi-centre evaluation of repeatability and reproducibility of the direct agglutination test for visceral leishmaniasis. Trop Med Int Health. 1999;4:31-7.
19. Schallig HD, Schoone GJ, Kroon CC, Hailu A, Chappuis F, Veeken H. Development and application of simple diagnostic tools for visceral leishmaniasis. Med Microbiol Immunol. 2001;190:69-71.
20. El Harith A, Kolk AH, Leeuwenburg J, Muigai R, Huigen E, Jelsma T, et al. Improvement of a direct agglutination test for field studies of visceral leishmaniasis. J Clin Microbiol. 1988;26:1321-5.
21. Meredith SE, Kroon NC, Sondorp E, Seaman J, Goris MG, van Ingen CW, et al. Leish kit, a stable direct agglutination test based on freeze-dried antigen for the serodiagnosis of visceral leishmaniasis. J Clin Microbiol .1995;33:1742-5.
22. Altman DG. Practical statistics for medical research. London: Chapman & Hall/CRC Press; 1991.
23. Bimar S, Das VN, Sinha PK, Verma N, Ranjan A, Singh SK, et al. Usefulness of the direct agglutination test in the early detection of subclinical Leishmania donovani infection:a community-based study. Ann Trop Med Parasitol. 2005;99:743-9.
24. Silva ES, Schoone GJ, Gontijo CM, Brazil RP, Pacheco RS, Schallig DF. Application of direct agglutination test (DAT) and fast agglutination screening test (FAST) for sero-diagnosis of visceral leishmaniasis in endemic area of Minas Gerais, Brazil. Kinetoplastid Bio Dis. 2005;4:4.
25. Hailu A. Pre and post-treatment antibody levels in visceral leishmaniasis. Trans R Soc Trop Med Hyg. 1990;84: 673-5.
26. Ponce C, Ponce E, Morrison A, Cruz A, Kreutzer R, MacMahon-Pratt D, et al. Leishmania donovani chagasi: new clinical variant of cutaneous leishmaniasis in Honduras. Lancet. 1991;337:67-70.
27. Stark D, Pett S, Marrito D, Harkness J. Post-kalaazar dermal leishmaniasis due to Leishmania infantum in a human immunodeficiency virus type 1-infected patient. J Clin Microbiol. 2006;44:1178-80.
28. Vasconcelos AB, Sousa AQ, Vasconcelos AW, Diogenes MJ, Mohen H, Grimaldi G Jr, et al. Parisitisme cutan par Leishmania (Leishmania) chagasi au cours de la leishmaniose viscrale Sud-Americaine.
Bull Soc Pathol Exot. 1993;86:101-5.
29. Convit, J, Ulrich M, Fernández CT, Tapia FJ, Cáceres-Dittmar G, Castés M, et al. The clinical and immunological spectrum of American cutaneous leishmaniasis. Trans R Soc Trop Med Hyg. 1993;87:444-8.
30. Gradoni L. Epizootiology of canine leishmaniasis in southern Europe. In: Killick Kendrick R, editor. Canine leishmaniasis an update. Wiesbaden: Hoeschst Roussel Vet; 1999. p.32-9.
31. Askford RW. Leishmaniasis reservoirs and their significance in control. Clin Dermatol. 1996;14:523-32.
32. Courtenay O, Quinnell RJ, Garcez LM, Shaw JJ, Dye C. Infectiousness in a cohort of Brazilian dogs: why culling fails to control visceral leishmaniasis in areas of high transmission. J Infect Dis. 2002;186:1314-20
33. Dantas-Torres F, Brandao-Filho SP. Visceral leishmaniasis in Brazil: revisiting paradigms of epidemiology and control. Rev Inst Med Trop Sao Paulo. 2006;48:151-6.
34. Cardoso L, Schallig HD, Neto F, Kroon N, Rodrigues M. Serological survey of Leishmania infection in dog from the municipality of Peso da Regua (Alto Douro, Portugal) using direct agglutination test (DAT) and fast agglutination test (FAST). Acta Trop. 2004;91:95-100.
35. Da Silva ES, van der Meide WF, Schoone GJ, Gontijo CM, Schallig HD, Brazil RP. Diagnosis of canine leishmaniasis in the endemic area of Belo Horizonte, Minas Gerais, Brazil by parasite, antibody and DNA detection assays. Vet Res Commun. 2006;30:637-43.
36. Neogy AB, Vouldoukis I, Silva OA, Tselentis Y, Lascombe JC, Segalen T, et al. Serodiagnosis and screening of canine visceral Leishmaniasis in an endemic area of Corsica: applicability of a direct agglutination test and immunoblot analysis. Am J Trop Med Hyg. 1992;47:772-7.
37. Oskam L, Slappendel RL, Beijer EG, Kroon NC, van Ingen CW, Ozensoy S, et al. Dog-DAT: a direct agglutination test using stabilized, freeze-dried antigen for the serodiagnosis of canine visceral leishmaniasis. FEMS Immunol Med Microbiol. 1996;16:235-9.
38. Garcez LM, Shaw JJ, Silveira FT. Direct agglutination test in the serodiagnosis of visceral leishmaniasis in the state of Para. Rev Soc Bras Med. 1996;29:165-80.
How to Cite
1.
Terán-Angel G, Schallig H, Zerpa O, Rodríguez V, Ulrich M, Cabrera M. The direct agglutination test as an alternative method for the diagnosis of canine and human visceral leishmaniasis. biomedica [Internet]. 2007 Sep. 1 [cited 2024 May 17];27(3):447-53. Available from: https://revistabiomedica.org/index.php/biomedica/article/view/207
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