Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-23T00:50:38.011Z Has data issue: false hasContentIssue false
  • English
  • Français

Geographical distribution and epidemiological features of Old World Leishmania infantum and Leishmania donovani foci, based on the isoenzyme analysis of 2277 strains

Published online by Cambridge University Press:  12 November 2012

FRANCINE PRATLONG ,
PATRICK LAMI ,
CHRISTOPHE RAVEL ,
YVES BALARD ,
JACQUES DEREURE ,
GHISLAINE SERRES ,
FOUAD EL BAIDOURI  and
JEAN-PIERRE DEDET
FRANCINE PRATLONG
Affiliation:
Université Montpellier 1 (UFR Médecine), Centre National de référence des leishmanioses, UMR «MIVEGEC» (CNRS 5290, IRD 224, UM1, UM2), Département de Parasitologie-Mycologie (Professeur Patrick Bastien), CHRU de Montpellier, 39, Avenue Charles Flahault, 34295 Montpellier Cedex 5, France
PATRICK LAMI
Affiliation:
Université Montpellier 1 (UFR Médecine), Centre National de référence des leishmanioses, UMR «MIVEGEC» (CNRS 5290, IRD 224, UM1, UM2), Département de Parasitologie-Mycologie (Professeur Patrick Bastien), CHRU de Montpellier, 39, Avenue Charles Flahault, 34295 Montpellier Cedex 5, France
CHRISTOPHE RAVEL
Affiliation:
Université Montpellier 1 (UFR Médecine), Centre National de référence des leishmanioses, UMR «MIVEGEC» (CNRS 5290, IRD 224, UM1, UM2), Département de Parasitologie-Mycologie (Professeur Patrick Bastien), CHRU de Montpellier, 39, Avenue Charles Flahault, 34295 Montpellier Cedex 5, France
YVES BALARD
Affiliation:
Université Montpellier 1 (UFR Médecine), Centre National de référence des leishmanioses, UMR «MIVEGEC» (CNRS 5290, IRD 224, UM1, UM2), Département de Parasitologie-Mycologie (Professeur Patrick Bastien), CHRU de Montpellier, 39, Avenue Charles Flahault, 34295 Montpellier Cedex 5, France
JACQUES DEREURE
Affiliation:
Université Montpellier 1 (UFR Médecine), Centre National de référence des leishmanioses, UMR «MIVEGEC» (CNRS 5290, IRD 224, UM1, UM2), Département de Parasitologie-Mycologie (Professeur Patrick Bastien), CHRU de Montpellier, 39, Avenue Charles Flahault, 34295 Montpellier Cedex 5, France
GHISLAINE SERRES
Affiliation:
Université Montpellier 1 (UFR Médecine), Centre National de référence des leishmanioses, UMR «MIVEGEC» (CNRS 5290, IRD 224, UM1, UM2), Département de Parasitologie-Mycologie (Professeur Patrick Bastien), CHRU de Montpellier, 39, Avenue Charles Flahault, 34295 Montpellier Cedex 5, France
FOUAD EL BAIDOURI
Affiliation:
Université Montpellier 1 (UFR Médecine), Centre National de référence des leishmanioses, UMR «MIVEGEC» (CNRS 5290, IRD 224, UM1, UM2), Département de Parasitologie-Mycologie (Professeur Patrick Bastien), CHRU de Montpellier, 39, Avenue Charles Flahault, 34295 Montpellier Cedex 5, France
JEAN-PIERRE DEDET*
Affiliation:
Université Montpellier 1 (UFR Médecine), Centre National de référence des leishmanioses, UMR «MIVEGEC» (CNRS 5290, IRD 224, UM1, UM2), Département de Parasitologie-Mycologie (Professeur Patrick Bastien), CHRU de Montpellier, 39, Avenue Charles Flahault, 34295 Montpellier Cedex 5, France
*
*Corresponding author: Département de Parasitologie-Mycologie, 39 avenue Charles Flahault, 34295 Montpellier Cedex 5, France. Tel: 334 67 33 23 50. Fax: 334 67 33 23 58. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

A series of 2277 Leishmania strains from Old World visceral leishmaniasis foci, isolated between 1973 and 2008, were studied by isoenzyme analysis. The strains were obtained from humans, domestic and wild carnivores, rodents and phlebotomine sandflies, and came from 36 countries. In all, 60 different zymodemes were identified and clustered by a phenetic analysis into 3 different groups corresponding to the typically visceralizing species L. donovani (20 zymodemes, 169 strains), L. archibaldi (3 zymodemes, 46 strains) and L. infantum (37 zymodemes, 2,062 strains). The taxonomic position of these isoenzymatic groups is discussed in view of contradictory results obtained from recent molecular studies.

Keywords

visceral leishmaniasisLeishmania infantumLeishmania donovaniLeishmania archibaldiisoenzymatic identificationOld World
Type
Research Article
Information
Parasitology , Volume 140 , Issue 4 , April 2013 , pp. 423 - 434
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abranches, P., Conceição-Silva, F. M., Ribeiro, M. M. S., Lopes, F. J. and Gomes, L. T. (1983). Kala-Azar in Portugal. IV. The wild reservoir: the isolates of a Leishmania from a fox. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 420–421.CrossRefGoogle ScholarPubMed
Aït Oudhia, K., Harrat, Z., Benikhlef, R., Dedet, J. P. and Pratlong, F. (2011). Canine Leishmania infantum enzymatic polymorphism: a review including 1023 strains of the Mediterranean area, with special reference to Algeria. Acta Tropica 118, 80–86.CrossRefGoogle ScholarPubMed
Alam, M. Z., Haralambous, C., Kuhls, K., Gouzelou, E., Sgouras, D., Soteriadou, K., Schnur, L., Pratlong, F., Schönian, G. (2009). The paraphyletic composition of Leishmania donovani zymodeme MON-37 revealed by multilocus microsatellite typing. Microbes and Infection 11, 707–715.CrossRefGoogle ScholarPubMed
Alam, M. Z., Kuhls, K., Schweynoch, C., Sundar, S., Rijal, S., Shamsuzzaman, A. K. M., Raju, B. V. S., Salotra, P., Dujardin, J. C. and Schönian, G. (2009). Multilocus microsatellite typing (MLMT) reveals genetic homogeneity of Leishmania donovani strains in the Indian subcontinent. Infection, Genetics and Evolution 9, 24–31.CrossRefGoogle ScholarPubMed
Antoniou, M., Haralambous, C., Mazeris, A., Pratlong, F., Dedet, J. P. and Soteriadou, K. (2008). Leishmania donovani causing visceral or cutaneous leishmaniasis in Europe: Cyprus evidence an alarm call. Lancet Infection 8, 5–6.Google ScholarPubMed
Belhadj, S., Pratlong, F., Toumi, N. H., Kallel, K., Mahjoub, H., Babba, H., Azaiez, R., Dedet, J. P. and Chaker, E. (2002). Visceral leishmaniasis in Tunisia : Result of the isoenzymatic characterization of 65 Leishmania infantum strains. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 627–630.CrossRefGoogle ScholarPubMed
Bettini, S., Pozio, E. and Gradoni, L. (1980). Leishmaniasis in Tuscany (Italy): II-Leishmania from wild Rodentia and Carnivora in a human and canine leishmaniasis focus. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 77–83.CrossRefGoogle Scholar
Campino, L., Pratlong, F., Abranches, P., Rioux, J. A., Santos-Gomes, G., Alves-Pires, C., Cortes, S., Ramada, J., Cristovao, J. M., Afonso, M. O. and Dedet, J. P. (2006). Leishmaniasis in Portugal: enzyme polymorphism of Leishmania infantum based on the identification of 213 strains. Tropical Medicine and International Health 11, 1708–1714.CrossRefGoogle ScholarPubMed
Castellani, A. and Chalmers, A. J. (1919). Manual of Tropical Medicine. 3rd Edn. Balliere Tindalle & Cox, London, UK.CrossRefGoogle Scholar
Chicharro, C., Jimenez, M. I. and Alvar, J. (2003). Iso-enzymatic variability of Leishmania infantum in Spain. Annals of Tropical Medicine and Parasitology 97, 57–64.CrossRefGoogle ScholarPubMed
Dedet, J. P. and Pratlong, F. (2009). Leishmaniasis. In Manson's Tropical Diseases (ed. Cook, G. C. and Zumla, A.), pp. 1341–1365. 22nd Edn. Elsevier Science Limited, Saunders, London, UK.CrossRefGoogle Scholar
Dereure, J., El Safi, S. H., Bucheton, B., Boni, M., Kheir, M. M., Davoust, B., Pratlong, F., Feugier, E., Lambert, M., Dessein, A. and Dedet, J. P. (2003). Visceral leishmaniasis in eastern Sudan: parasite identification in humans and dogs; host-parasite relationships. Microbes & Infection 5, 1103–1108.CrossRefGoogle ScholarPubMed
Downing, T., Stark, O., Vanaerschot, M., Imamura, H., Sanders, M., Decuypere, S., De Doncker, S., Maes, I., Rijal, S., Sundar, S., Dujardin, J. C., Berriman, M. and Schönian, G. (2012). Genome-wide SNP and microsatellite variation illumate population-level epidemiology in the Leishmania donovani species compex. Infection, Genetics and Evolution 12, 149–159.CrossRefGoogle Scholar
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
Felsenstein, J. (2004). PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, USA.Google Scholar
Gelanew, T., Kuhls, K., Hurissa, Z., Weldegebreal, T., Hailu, W., Kassahun, A., Abebe, T., Hailu, A. and Schönian, G. (2010). Inference of population structure of Leishmania donovani strains isolated from different Ethiopian visceral leishmaniasis endemic areas. PLoS Neglected Tropical Diseases 4, e889.CrossRefGoogle ScholarPubMed
Gramiccia, M. (2003). The identification and variability of the parasites causing leishmaniasis in HIV-positive patients in Italy. Annals of Tropical Medicine and Parasitology 97 (Suppl 1), 65–73.CrossRefGoogle ScholarPubMed
Gramiccia, M., Gradoni, L. and Troiani, M. (1992). HIV-Leishmania co-infections in Italy. Isoenzyme characterization of Leishmania causing visceral leishmaniasis in HIV patients. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 161–163.CrossRefGoogle ScholarPubMed
Gramiccia, M., Gradoni, L. and Troiani, M. (1995). Heterogeneity among zymodemes of Leishmania infantum from HIV-positive patients with visceral leishmaniasis in south Italy. FEMS Microbiology Letters 28, 33–38.CrossRefGoogle Scholar
Harrat, Z., Pratlong, F., Belazzoug, S., Dereure, J., Deniau, M., Rioux, J. A., Belkaid, M. and Dedet, J. P. (1996). Leishmania infantum and L. major in Algeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 625–629.CrossRefGoogle ScholarPubMed
Jamjoom, M. B., Ashford, R. W., Bates, P. A., Chance, M. L., Kemp, S. J., Watts, P. C. and Noyes, H. A. (2004). Leishmania donovani is the only cause of visceral leishmaniasis in East Africa; previous descriptions of L. infantum and ‘L. archibaldi’ from this region are a consequence of convergent evolution in the isoenzyme data. Parasitology 129, 1–11.CrossRefGoogle ScholarPubMed
Jiménez, M., Ferrel-Dufol, M., Canavate, C., Gutierrez-Solar, B., Molina, R., Laguna, F., Lopez-Velez, R., Cercenado, E., Daudén, E., Blazquez, J., Ladron de Gevara, C., Gomez, J., De la Torre, J., Barros, C., Altes, J., Cerra, T. and Alvar, J. (1995). Varability of Leishmania (Leishmania) infantum among stocks from immunocompromised, immunocompetent patients and dogs in Spain. FEMS Microbiology Letters 131, 197–204.CrossRefGoogle Scholar
Kallel, K., Haouas, N., Pratlong, F., Kaouech, E., Belhadj, S., Anane, S., Dedet, J. P., Babba, H. and Chaker, E. (2008). La leishmaniose cutanée due à Leishmania infantum MON-24 en Tunisie: extension du foyer vers le centre du pays. Bulletin de la Société de Pathologie exotique 101, 30–31.Google Scholar
Karunaweera, N. D., Pratlong, F., Siriwardan, H. V. Y. D., Ihalamulla, R. L. and Dedet, J. P. (2003). Sri Lankan cutaneous leishmaniasis is caused by Leishmania donovani, zymodeme MON-37. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 380–381.CrossRefGoogle ScholarPubMed
Kuhls, K., Keilonat, L., Ochsenreither, S., Chaar, M., Schweynoch, C., Presber, W. and Schönian, G. (2007). Multilocus microsatellite typing (MLMT) reveals genetically isolated populations between and within the main endemic regions of visceral leishmaniasis. Microbes and Infection 9, 334–343.CrossRefGoogle ScholarPubMed
Lanotte, G., Rioux, J. A., Maazoun, R., Pasteur, N., Pratlong, F. and Lepart, J. (1981). Application de la méthode numérique à la taxonomie du genre Leishmania Ross, 1903. A propos de 146 souches originaires de l'Ancien Monde. Utilisation des allozymes. Corollaires épidémiologiques et phylétiques. Annales de Parasitologie Humaine et Comparée 56, 575–592.CrossRefGoogle Scholar
Laveran, A. and Mesnil, F. (1903). Sur un protozoaire nouveau (Piroplasma donovani Lav. et Mesn.) parasite d'une fièvre de l'Inde. Comptes-Rendus de l'Académie des Sciences 137, 957–961.Google Scholar
Lukes, J., Mauricio, I. L., Schönian, G., Dujardin, J. C., Soteriadou, K., Dedet, J. P., Kuhls, K., Tintaya, W. Q., Jirku, M., Chocholova, E., Haralambous, C., Pratlong, F., Obornik, M., Horak, A., Ayala, F. J. and Miles, M. A. (2007). Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proceedings of the National Academy of Sciences, USA 104, 9375–9380.CrossRefGoogle ScholarPubMed
Martínez-Calvillo, S., Stuart, K. and Myler, P. J. (2005). Ploidy changes associated with disruption of two adjacent genes on Leishmania major chromosome 1. International Journal for Parasitology 35, 419–429.CrossRefGoogle ScholarPubMed
Martin-Sanchez, J., Gramiccia, M., Di Muccio, T., Ludovisi, A. and Morillas-Márquez, F. (2004). Isoenzymatic polymorphism of Leishmania infantum in southern Spain. Transactions of the Royal Society of Tropical Medicine and Hygiene 98, 228–232.CrossRefGoogle ScholarPubMed
Martin-Sanchez, J., Morillas-Márquez, F., Acedo-Sánchez, C. and Sanchez-Marín, M. C. (1995). The variability of the etiological agent of leishmaniasis in the North-East of the Almeria region, South-east Spain. Systematic Parasitology 30, 233–238.CrossRefGoogle Scholar
Marty, P., Izri, A., Ozon, C., Haas, P., Rosenthal, E., Del Giudice, P., Godenir, J., Coulibaly, E., Gari-Toussaint, M., Delaunay, P., Ferrua, B., Haas, H., Pratlong, F. and Le Fichoux, Y. (2007). A century of leishmaniasis in Alpes-Maritimes, France. Annals of Tropical Medicine and Parasitology 101, 563–574.CrossRefGoogle ScholarPubMed
Mauricio, I. L., Yeo, M., Baghaei, M., Doto, D., Pratlong, F., Zemanoca, E., Dedet, J. P., Lukes, J. and Miles, M. A. (2006). Towards multilocus sequence typing of the Leishmania donovani complex: resolving genotypes and haplotypes for five polymorphic metabolic enzymes (ASAT, GPI, NH1, NH2, PGD). International Journal for Parasitology 36, 757–769.CrossRefGoogle ScholarPubMed
Moreno, G., Rioux, J. A., Lanotte, G., Pratlong, F. and Serres, E. (1986). Le complexe Leishmania donovani s.l. Analyse enzymatique et traitement numérique. Individualisation du complexe Leishmania infantum. Corollaires biogéo-graphiques et phylétiques. A propos de 146 souches originaires de l'Ancien et du Nouveau Monde. In Leishmania. Taxonomie et Phylogenèse. Applications Eco-épidémiologiques (ed. Rioux, J. A.), pp. 105–117. IMEEE, Montpellier, France.Google Scholar
Nicolle, C. (1908). Sur trois cas d'infection splénique infantile à corps de Leishman observés en Tunisie. Archives de l'Institut Pasteur de Tunis 3, 1–26.Google Scholar
Piarroux, R., Trouvé, V., Pratlong, F., Martini, A., Lambert, M. and Rioux, J. A. (1994). The use of isoelectric focusing on polyacrylamide gel for the enzymatic analysis of Old World Leishmania species. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 475–478.CrossRefGoogle ScholarPubMed
Portus, M., Gallego, M., Riera, C., Aisa, M. J., Fisa, R. and Castillejo, S. (2002). Wild and domestic mammals in the life cycle of Leishmania infantum in Southwest Europe. A literature review and studies performed in Catalonia (Spain). Revista Iberica de Parasitologia 62, 72–76.Google Scholar
Pratlong, F., Dereure, J., Bucheton, B., El-Safi, S., Dessein, A., Lanotte, G. and Dedet, J. P. (2001). Sudan: the possible original focus of visceral leishmaniasis. Parasitology 122, 599–605.CrossRefGoogle ScholarPubMed
Pratlong, F., Dereure, J., Deniau, M., Marty, P., Faraut-Gambarelli, F. and Dedet, J. P. (2003). Enzymatic polymorphism during Leishmania/HIV co-infection. Study of 381 Leishmania strains received between 1986 and 2000 at the International Cryobank of Montpellier (France). Annals of Tropical Medicine and Parasitology 97, S47–S56.CrossRefGoogle ScholarPubMed
Pratlong, F., Dereure, J., Ravel, C., Lami, P., Balard, Y., Serres, G., Lanotte, G., Rioux, J. A. and Dedet, J. P. (2009). Geographical distribution and epidemiological features of Old World cutaneous leishmaniasis foci, based on the isoenzyme analysis of 1048 strains. Tropical Medicine and International Health 14, 1071–1085.CrossRefGoogle ScholarPubMed
Pratlong, F., Bastien, P., Perello, R., Lami, P. and Dedet, J. P. (1995). Human cutaneous leishmaniasis caused by Leishmania donovani sensu stricto in Yemen. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 398–399.CrossRefGoogle ScholarPubMed
Pratlong, F., Rioux, J. A., Marty, P., Faraut-Gambarelli, F., Dereure, J., Lanotte, G. and Dedet, J. P. (2004). Isoenzymatic analysis of 712 strains of Leishmania infantum in the South of France and relationship of enzymatic polymorphism to clinical and epidemiological features. Journal of Clinical Microbiology 42, 4077–4082.CrossRefGoogle ScholarPubMed
Rioux, J. A., Albaret, J. L., Houin, R., Dedet, J. P. and Lanotte, G. (1968). Ecologie des leishmanioses dans le sud de la France. 2.- Les réservoirs selvatiques. Infestation spontanée du renard (Vulpes vulpes L.). Annales de Parasitologie Humaine et Comparée 43, 421–428.CrossRefGoogle Scholar
Rioux, J. A., Lanotte, G., Pratlong, F., Bastien, P. and Perieres, J. (1990). Taxonomy of Leishmania. Use of isoenzymes. Suggestion for a new classification. Annales de Parasitologie Humaine et Comparée 65, 111–115.CrossRefGoogle ScholarPubMed
Rougeron, V., De Meeûs, T., Hide, M., Le Falher, G., Bucheton, B., Dereure, J., El-Safi, S. H., Dessein, A. and Banyuls, A. L. (2011). Multifaceted population structure and reproductive strategy in Leishmania donovani complex in one Sudanese village. PLOS Neglected tropical Diseases 5, 1–11.CrossRefGoogle ScholarPubMed
Schönian, G., Mauricio, I. and Cupolillo, E. (2010). Is it time to revise the nomenclature of Leishmania? Trends in Parasitology 26, 466–469.CrossRefGoogle ScholarPubMed
Thakur, C. P., Dedet, J. P., Narain, S. and Pratlong, F. (2001). Leishmania species, drug unresponsiveness and visceral leishmaniasis in Bihar, India. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 187–189.CrossRefGoogle ScholarPubMed
Van der Auwera, G., Fraga, J., Montalvo, A. M. and Dujardin, J. C. (2011). Leishmania taxonomy up for promotion? Trends in Parasitology 27, 49–50.CrossRefGoogle ScholarPubMed
Zemanová, E., Jirku, M., Mauricio, I. L., Horák, A., Miles, M. A. and Lukes, J. (2007). The Leishmania donovani complex: genotypes of five metabolic enzymes (ICD, ME, MPI, G6PDH, and FH), new targets for multilocus sequence typing. International Journal for Parasitology 37, 149–160.CrossRefGoogle ScholarPubMed