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Abstract

Background

A large outbreak of leishmaniasis with 758 cutaneous and visceral leishmaniasis cases occurred in 2009 in Fuenlabrada, in the south-west of the Madrid region of Spain.

Aim

We aimed to determine the prevalence of asymptomatic infection after this outbreak, and its associated risk factors.

Methods

A cross-sectional study of 804 healthy individuals living in Fuenlabrada who had no history of leishmaniasis, was conducted between January and July 2015. Asymptomatic infections were sought by either a combination of PCR, immunofluorescent antibody titre, and direct agglutination tests, or by whole blood stimulation assay (WBA) with interleukin-2 (IL-2) quantification.

Results

Using the first approach, prevalence of asymptomatic individuals was 1.1% (9/804), while the second returned a value of 20.7% (143/804). Older age, being male, proximity to the park where the focus of infection was identified, and living in a detached house, were all strongly associated with the prevalence of asymptomatic infection.

Conclusions

The true number of infected individuals may be underestimated if only serological methods are used. The combination of WBA with IL-2 quantification may allow to better determine the prevalence of asymptomatic infection, which would be useful in establishing control measures and in quantifying their impact. In our study, the use of WBA with IL-2 quantification also helped establish the risk factors that influence exposure to and infection by .

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/content/10.2807/1560-7917.ES.2019.24.22.1800379
2019-05-30
2024-04-25
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.22.1800379
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References

  1. World Health Organization. Control of the leishmaniases. World Health Organ Tech Rep Ser. 2010; (949):xii-xiii, 1-186, back cover. PMID: 21485694 
  2. Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 2012;7(5):e35671.  https://doi.org/10.1371/journal.pone.0035671  PMID: 22693548 
  3. Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, et al. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol. 2007;5(11):873-82.  https://doi.org/10.1038/nrmicro1748  PMID: 17938629 
  4. Topno RK, Das VN, Ranjan A, Pandey K, Singh D, Kumar N, et al. Asymptomatic infection with visceral leishmaniasis in a disease-endemic area in bihar, India. Am J Trop Med Hyg. 2010;83(3):502-6.  https://doi.org/10.4269/ajtmh.2010.09-0345  PMID: 20810810 
  5. Bern C, Haque R, Chowdhury R, Ali M, Kurkjian KM, Vaz L, et al. The epidemiology of visceral leishmaniasis and asymptomatic leishmanial infection in a highly endemic Bangladeshi village. Am J Trop Med Hyg. 2007;76(5):909-14.  https://doi.org/10.4269/ajtmh.2007.76.909  PMID: 17488915 
  6. Ostyn B, Gidwani K, Khanal B, Picado A, Chappuis F, Singh SP, et al. Incidence of symptomatic and asymptomatic Leishmania donovani infections in high-endemic foci in India and Nepal: a prospective study. PLoS Negl Trop Dis. 2011;5(10):e1284.  https://doi.org/10.1371/journal.pntd.0001284  PMID: 21991397 
  7. Stauch A, Sarkar RR, Picado A, Ostyn B, Sundar S, Rijal S, et al. Visceral leishmaniasis in the Indian subcontinent: modelling epidemiology and control. PLoS Negl Trop Dis. 2011;5(11):e1405.  https://doi.org/10.1371/journal.pntd.0001405  PMID: 22140589 
  8. Michel G, Pomares C, Ferrua B, Marty P. Importance of worldwide asymptomatic carriers of Leishmania infantum (L. chagasi) in human. Acta Trop. 2011;119(2-3):69-75.  https://doi.org/10.1016/j.actatropica.2011.05.012  PMID: 21679680 
  9. Babuadze G, Alvar J, Argaw D, de Koning HP, Iosava M, Kekelidze M, et al. Epidemiology of visceral leishmaniasis in Georgia. PLoS Negl Trop Dis. 2014;8(3):e2725.  https://doi.org/10.1371/journal.pntd.0002725  PMID: 24603768 
  10. EL-Safi SH, Bucheton B, Kheir MM, Musa HA, EL-Obaid M, Hammad A, et al. Epidemiology of visceral leishmaniasis in Atbara River area, eastern Sudan: the outbreak of Barbar El Fugara village (1996-1997). Microbes Infect. 2002;4(14):1439-47. PMID: 12475634 
  11. Marty P, Izri A, Ozon C, Haas P, Rosenthal E, Del Giudice P, et al. A century of leishmaniasis in Alpes-Maritimes, France. Ann Trop Med Parasitol. 2007;101(7):563-74.  https://doi.org/10.1179/136485907X229121  PMID: 17877875 
  12. Costa CH, Stewart JM, Gomes RB, Garcez LM, Ramos PK, Bozza M, et al. Asymptomatic human carriers of Leishmania chagasi. Am J Trop Med Hyg. 2002;66(4):334-7.  https://doi.org/10.4269/ajtmh.2002.66.334  PMID: 12164285 
  13. Hailu A, Gramiccia M, Kager PA. Visceral leishmaniasis in Aba-Roba, south-western Ethiopia: prevalence and incidence of active and subclinical infections. Ann Trop Med Parasitol. 2009;103(8):659-70.  https://doi.org/10.1179/000349809X12554106963555  PMID: 20030990 
  14. Werneck GL, Rodrigues L Jr, Santos MV, Araújo IB, Moura LS, Lima SS, et al. The burden of Leishmania chagasi infection during an urban outbreak of visceral leishmaniasis in Brazil. Acta Trop. 2002;83(1):13-8.  https://doi.org/10.1016/S0001-706X(02)00058-X  PMID: 12062788 
  15. Ibarra-Meneses AV, Carrillo E, Sánchez C, García-Martínez J, López Lacomba D, San Martin JV, et al. Interleukin-2 as a marker for detecting asymptomatic individuals in areas where Leishmania infantum is endemic. Clin Microbiol Infect. 2016;22(8):739.e1-4.  https://doi.org/10.1016/j.cmi.2016.05.021  PMID: 27265372 
  16. Ibarra-Meneses AV, Ghosh P, Hossain F, Chowdhury R, Mondal D, Alvar J, et al. IFN-γ, IL-2, IP-10, and MIG as Biomarkers of Exposure to Leishmania spp., and of Cure in Human Visceral Leishmaniasis. Front Cell Infect Microbiol. 2017;7:200.  https://doi.org/10.3389/fcimb.2017.00200  PMID: 28620584 
  17. Ibarra-Meneses AV, Sanchez C, Alvar J, Moreno J, Carrillo E. Monocyte Chemotactic Protein 1 in Plasma from Soluble Leishmania Antigen-Stimulated Whole Blood as a Potential Biomarker of the Cellular Immune Response to Leishmania infantum. Front Immunol. 2017;8:1208.  https://doi.org/10.3389/fimmu.2017.01208  PMID: 29033933 
  18. Gidwani K, Jones S, Kumar R, Boelaert M, Sundar S. Interferon-gamma release assay (modified QuantiFERON) as a potential marker of infection for Leishmania donovani, a proof of concept study. PLoS Negl Trop Dis. 2011;5(4):e1042.  https://doi.org/10.1371/journal.pntd.0001042  PMID: 21526219 
  19. Turgay N, Balcioglu IC, Toz SO, Ozbel Y, Jones SL. Quantiferon-Leishmania as an epidemiological tool for evaluating the exposure to Leishmania infection. Am J Trop Med Hyg. 2010;83(4):822-4.  https://doi.org/10.4269/ajtmh.2010.09-0605  PMID: 20889872 
  20. Gradoni L, Rogelio López-Vélez R, Mokni M. Manual on case management and surveillance of the leishmaniases in the WHO European Region. Copenhagen: World Health Organization Regional Office for Europe. 2017. Available from: http://www.euro.who.int/en/publications/abstracts/manual-on-case-management-and-surveillance-of-the-leishmaniases-in-the-who-european-region-2017
  21. Arce A, Estirado A, Ordobas M, Sevilla S, García N, Moratilla L, et al. Re-emergence of leishmaniasis in Spain: community outbreak in Madrid, Spain, 2009 to 2012. Euro Surveill. 2013;18(30):20546.  https://doi.org/10.2807/1560-7917.ES2013.18.30.20546  PMID: 23929177 
  22. González E, Jiménez M, Hernández S, Martín-Martín I, Molina R. Phlebotomine sand fly survey in the focus of leishmaniasis in Madrid, Spain (2012-2014): seasonal dynamics, Leishmania infantum infection rates and blood meal preferences. Parasit Vectors. 2017;10(1):368.  https://doi.org/10.1186/s13071-017-2309-z  PMID: 28764772 
  23. Comunidad de Madrid. Epidemiological bulletin of the Community of Madrid. Madrid: Community of Madrid. Dec 2017;12(23):41. Spanish. Available from: http://www.madrid.org/bvirtual/BVCM020201.pdf
  24. de Ruiter CM, van der Veer C, Leeflang MM, Deborggraeve S, Lucas C, Adams ER. Molecular tools for diagnosis of visceral leishmaniasis: systematic review and meta-analysis of diagnostic test accuracy. J Clin Microbiol. 2014;52(9):3147-55.  https://doi.org/10.1128/JCM.00372-14  PMID: 24829226 
  25. Bray RS. Leishmaniasis. In: Houba V, ed. Immunological investigation of tropical parasitic diseases. Edinburgh: Churchill Livingstone; 1980:65-74.
  26. Cortes S, Rolão N, Ramada J, Campino L. PCR as a rapid and sensitive tool in the diagnosis of human and canine leishmaniasis using Leishmania donovani s.l.-specific kinetoplastid primers. Trans R Soc Trop Med Hyg. 2004;98(1):12-7.  https://doi.org/10.1016/S0035-9203(03)00002-6  PMID: 14702834 
  27. Carrillo E, Carrasco-Antón N, López-Medrano F, Salto E, Fernández L, San Martín JV, et al. Cytokine Release Assays as Tests for Exposure to Leishmania, and for Confirming Cure from Leishmaniasis, in Solid Organ Transplant Recipients. PLoS Negl Trop Dis. 2015;9(10):e0004179.  https://doi.org/10.1371/journal.pntd.0004179  PMID: 26496365 
  28. Ready PD. Leishmaniasis emergence in Europe. Euro Surveill. 2010;15(10):19505. PMID: 20403308 
  29. Srivastava P, Dayama A, Mehrotra S, Sundar S. Diagnosis of visceral leishmaniasis. Trans R Soc Trop Med Hyg. 2011;105(1):1-6.  https://doi.org/10.1016/j.trstmh.2010.09.006  PMID: 21074233 
  30. Singh DP, Goyal RK, Singh RK, Sundar S, Mohapatra TM. In search of an ideal test for diagnosis and prognosis of kala-azar. J Health Popul Nutr. 2010;28(3):281-5. PMID: 20635639 
  31. do Rêgo Lima LV, Santos Ramos PK, Campos MB, dos Santos TV, de Castro Gomes CM, Laurenti MD, et al. Preclinical diagnosis of American visceral leishmaniasis during early onset of human Leishmania (L.) infantum chagasi-infection. Pathog Glob Health. 2014;108(8):381-4.  https://doi.org/10.1179/2047773214Y.0000000166  PMID: 25491437 
  32. Kyriakou DS, Alexandrakis MG, Passam FH, Kourelis TV, Foundouli P, Matalliotakis E, et al. Quick detection of Leishmania in peripheral blood by flow cytometry. Is prestorage leucodepletion necessary for leishmaniasis prevention in endemic areas? Transfus Med. 2003;13(2):59-62.  https://doi.org/10.1046/j.1365-3148.2003.00420.x  PMID: 12694549 
  33. Jimenez-Marco T, Fisa R, Girona-Llobera E, Cancino-Faure B, Tomás-Pérez M, Berenguer D, et al. Transfusion-transmitted leishmaniasis: a practical review. Transfusion. 2016;56(Suppl 1):S45-51.  https://doi.org/10.1111/trf.13344  PMID: 27001361 
  34. le Fichoux Y, Quaranta JF, Aufeuvre JP, Lelievre A, Marty P, Suffia I, et al. Occurrence of Leishmania infantum parasitemia in asymptomatic blood donors living in an area of endemicity in southern France. J Clin Microbiol. 1999;37(6):1953-7. PMID: 10325353 
  35. Scarlata F, Vitale F, Saporito L, Reale S, Vecchi VL, Giordano S, et al. Asymptomatic Leishmania infantum/chagasi infection in blood donors of western Sicily. Trans R Soc Trop Med Hyg. 2008;102(4):394-6.  https://doi.org/10.1016/j.trstmh.2008.01.011  PMID: 18321542 
  36. Fakhar M, Motazedian MH, Hatam GR, Asgari Q, Kalantari M, Mohebali M. Asymptomatic human carriers of Leishmania infantum: possible reservoirs for Mediterranean visceral leishmaniasis in southern Iran. Ann Trop Med Parasitol. 2008;102(7):577-83.  https://doi.org/10.1179/136485908X337526  PMID: 18817598 
  37. Ferreira GR, Castelo Branco Ribeiro JC, Meneses Filho A, de Jesus Cardoso Farias Pereira T, Parente DM, Pereira HF, et al. Human Competence to Transmit Leishmania infantum to Lutzomyia longipalpis and the Influence of Human Immunodeficiency Virus Infection. Am J Trop Med Hyg. 2018;98(1):126-33.  https://doi.org/10.4269/ajtmh.16-0883  PMID: 29141704 
  38. van Griensven J, Carrillo E, López-Vélez R, Lynen L, Moreno J. Leishmaniasis in immunosuppressed individuals. Clin Microbiol Infect. 2014;20(4):286-99.  https://doi.org/10.1111/1469-0691.12556  PMID: 24450618 
  39. Pampiglione S, Manson-Bahr PE, La Placa M, Borgatti MA, Musumeci S. Studies in Mediterranean leishmaniasis. 3. The leishmanin skin test in kala-azar. Trans R Soc Trop Med Hyg. 1975;69(1):60-8.  https://doi.org/10.1016/0035-9203(75)90012-7  PMID: 1145719 
  40. Custodio E, Gadisa E, Sordo L, Cruz I, Moreno J, Nieto J, et al. Factors associated with Leishmania asymptomatic infection: results from a cross-sectional survey in highland northern Ethiopia. PLoS Negl Trop Dis. 2012;6(9):e1813.  https://doi.org/10.1371/journal.pntd.0001813  PMID: 23029576 
  41. Killick-Kendrick R, Wilkes TJ, Alexander J, Bray RS, Rioux JA, Bailly H. The distance of attraction of CDC light traps to Phlebotomine sandflies. Ann Parasitol Hum Comp. 1985;60(6):763-7.  https://doi.org/10.1051/parasite/1985606763 
  42. Bart A, van Thiel PP, de Vries HJ, Hodiamont CJ, Van Gool T. Imported leishmaniasis in the Netherlands from 2005 to 2012: epidemiology, diagnostic techniques and sequence-based species typing from 195 patients. Euro Surveill. 2013;18(30):20544.  https://doi.org/10.2807/1560-7917.ES2013.18.30.20544  PMID: 23929178 
  43. Lawn SD, Whetham J, Chiodini PL, Kanagalingam J, Watson J, Behrens RH, et al. New world mucosal and cutaneous leishmaniasis: an emerging health problem among British travellers. QJM. 2004;97(12):781-8.  https://doi.org/10.1093/qjmed/hch127  PMID: 15569809 
  44. Di Muccio T, Scalone A, Bruno A, Marangi M, Grande R, Armignacco O, et al. Epidemiology of Imported Leishmaniasis in Italy: Implications for a European Endemic Country. PLoS One. 2015;10(6):e0129418.  https://doi.org/10.1371/journal.pone.0129418  PMID: 26114938 
  45. Söbirk SK, Inghammar M, Collin M, Davidsson L. Imported leishmaniasis in Sweden 1993-2016. Epidemiol Infect. 2018;146(10):1267-74.  https://doi.org/10.1017/S0950268818001309  PMID: 29848389 
Prevalence of asymptomatic Leishmania infection and associated risk factors, after an outbreak in the south-western Madrid region, Spain, 2015
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Ana+Victoria+Ibarra-Meneses&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ibarra-Meneses Ana Victoria</a>, <a href="/search?value1=Eugenia+Carrillo&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Carrillo Eugenia</a>, <a href="/search?value1=Javier+Nieto&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Nieto Javier</a>, <a href="/search?value1=Carmen+S%C3%A1nchez&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sánchez Carmen</a>, <a href="/search?value1=Sheila+Ortega&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ortega Sheila</a>, <a href="/search?value1=Alicia+Estirado&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Estirado Alicia</a>, <a href="/search?value1=Pello++Latasa+Zamalloa&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Latasa Zamalloa Pello </a>, <a href="/search?value1=Juan+Carlos+Sanz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sanz Juan Carlos</a>, <a href="/search?value1=Luis+Garc%C3%ADa-Comas&option1=author&noRedirect=true" class="nonDisambigAuthorLink">García-Comas Luis</a>, <a href="/search?value1=Mar%C3%ADa+Ordob%C3%A1s&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ordobás María</a>, <a href="/search?value1=Javier+Moreno&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Moreno Javier</a></span>. Prevalence of asymptomatic Leishmania infection and associated risk factors, after an outbreak in the south-western Madrid region, Spain, 2015. <a href="/content/ecdc">Euro Surveill.</a> 2019;24(22):pii=1800379. <a href="https://doi.org/10.2807/1560-7917.ES.2019.24.22.1800379" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2019.24.22.1800379</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 06 Jul 2018;&nbsp;&nbsp; <span class="generated">Accepted</span>: 10 Feb 2019 </span> </p>
/content/10.2807/1560-7917.ES.2019.24.22.1800379
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