Document Type : Review Article

Author

Dept. of Laboratory Science, Faculty of Paraveterinary Sciences, Bu-Ali Sina University, Hamadan, Iran

Abstract

Leishmaniasis is a disease caused by a malaria-like parasite called Leishmania in human and some species of animals. Detection of leishmaniasis has always been crucial for control and treatment of the disease. Different strategies have been approached for detection of leishmania. In this review methods used for detection of leishmania infection have been discussed and compared.

Keywords

Abdallah KA, Nour BY, Schallig HD, Mergani A, Hamid Z, Elkarim AA, Saeed OK,  Mohamadani AA (2004) Evaluation of the direct agglutination test based on freeze-dried Leishmania donovani promastigotes for the serodiagnosis of visceral leishmaniasis in Sudanese patients.Trop Med Int Health 9:1127-1131.
Agwale SM, Duhlinska DD,  Grimaldi Junior G (1998) Response to heterologous leishmanins in cutaneous leishmaniasis in Nigeria--discovery of a new focus.Mem Inst Oswaldo Cruz 93:23-27.
Ahluwalia IB, Bern C, Costa C, Akter T, Chowdhury R, Ali M, Alam D, Kenah E, Amann J, Islam M, Wagatsuma Y, Haque R, Breiman RF,  Maguire JH (2003) Visceral leishmaniasis: consequences of a neglected disease in a Bangladeshi community.Am J Trop Med Hyg 69:624-628.
Al-Hucheimi SN, Sultan BA,  Al-Dhalimi MA (2009) A comparative study of the diagnosis of Old World cutaneous leishmaniasis in Iraq by polymerase chain reaction and microbiologic and histopathologic methods.Int J Dermatol 48:404-408.
Allahverdiyev AM, Bagirova M, Uzun S, Alabaz D, Aksaray N, Kocabas E,  Koksal F (2005) The value of a new microculture method for diagnosis of visceral leishmaniasis by using bone marrow and peripheral blood.Am J Trop Med Hyg 73:276-280.
Alvar J, Aparicio P, Aseffa A, Den Boer M, Canavate C, Dedet JP, Gradoni L, Ter Horst R, Lopez-Velez R,  Moreno J (2008) The relationship between leishmaniasis and AIDS: the second 10 years.Clin Microbiol Rev 21:334-359, table of contents.
Alvar J, Bashaye S, Argaw D, Cruz I, Aparicio P, Kassa A, Orfanos G, Parreno F, Babaniyi O, Gudeta N, Canavate C,  Bern C (2007) Kala-azar outbreak in Libo Kemkem, Ethiopia: epidemiologic and parasitologic assessment.Am J Trop Med Hyg 77:275-282.
Alvar J, Canavate C, Gutierrez-Solar B, Jimenez M, Laguna F, Lopez-Velez R, Molina R,  Moreno J (1997) Leishmania and human immunodeficiency virus coinfection: the first 10 years.Clin Microbiol Rev 10:298-319.
Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J,  den Boer M (2012) Leishmaniasis worldwide and global estimates of its incidence.PLoS One 7:e35671.
Alvar J, Yactayo S,  Bern C (2006) Leishmaniasis and poverty.Trends Parasitol 22:552-557.
Andresen K, Gaafar A, El-Hassan AM, Ismail A, Dafalla M, Theander TG,  Kharazmi A (1996) Evaluation of the polymerase chain reaction in the diagnosis of cutaneous leishmaniasis due to Leishmania major: a comparison with direct microscopy of smears and sections from lesions.Trans R Soc Trop Med Hyg 90:133-135.
Aransay AM, Scoulica E,  Tselentis Y (2000) Detection and identification of Leishmania DNA within naturally infected sand flies by seminested PCR on minicircle kinetoplastic DNA.Appl Environ Microbiol 66:1933-1938.
Ashford RW (2000) The leishmaniases as emerging and reemerging zoonoses.Int J Parasitol 30:1269-1281.
Attar ZJ, Chance ML, el-Safi S, Carney J, Azazy A, El-Hadi M, Dourado C,  Hommel M (2001) Latex agglutination test for the detection of urinary antigens in visceral leishmaniasis.Acta Trop 78:11-16.
Aviles H, Belli A, Armijos R, Monroy FP,  Harris E (1999) PCR detection and identification of Leishmania parasites in clinical specimens in Ecuador: a comparison with classical diagnostic methods.J Parasitol 85:181-187.
Banuls AL, Dujardin JC, Guerrini F, De Doncker S, Jacquet D, Arevalo J, Noel S, Le Ray D,  Tibayrenc M (2000) Is Leishmania (Viannia) peruviana a distinct species? A MLEE/RAPD evolutionary genetics answer.J Eukaryot Microbiol 47:197-207.
Barnett PG, Singh SP, Bern C, Hightower AW,  Sundar S (2005) Virgin soil: the spread of visceral leishmaniasis into Uttar Pradesh, India.Am J Trop Med Hyg 73:720-725.
Bastrenta B, Buitrago R, Vargas F, Le Pont F, Torrez M, Flores M, Mita N,  Breniere SF (2002) First evidence of transmission of Leishmania (Viannia) lainsoni in a Sub Andean region of Bolivia.Acta Trop 83:249-253.
Bates PA (2007) Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies.Int J Parasitol 37:1097-1106.
Bensoussan E, Nasereddin A, Jonas F, Schnur LF,  Jaffe CL (2006) Comparison of PCR assays for diagnosis of cutaneous leishmaniasis.J Clin Microbiol 44:1435-1439.
Berhe N, Wolday D, Hailu A, Abraham Y, Ali A, Gebre-Michael T, Desjeux P, Sonnerborg A, Akuffo H,  Britton S (1999) HIV viral load and response to antileishmanial chemotherapy in co-infected patients.AIDS 13:1921-1925.
Berman JD (1997) Human leishmaniasis: clinical, diagnostic, and chemotherapeutic developments in the last 10 years.Clin Infect Dis 24:684-703.
Bern C, Hightower AW, Chowdhury R, Ali M, Amann J, Wagatsuma Y, Haque R, Kurkjian K, Vaz LE, Begum M, Akter T, Cetre-Sossah CB, Ahluwalia IB, Dotson E, Secor WE, Breiman RF,  Maguire JH (2005) Risk factors for kala-azar in Bangladesh.Emerg Infect Dis 11:655-662.
Bhargava P,  Singh R (2012) Developments in diagnosis and antileishmanial drugs.Interdiscip Perspect Infect Dis 2012:626838.
Bhattacharya SK, Sur D,  Karbwang J (2006) Childhood visceral leishmaniasis.Indian J Med Res 123:353-356.
Boarino A, Scalone A, Gradoni L, Ferroglio E, Vitale F, Zanatta R, Giuffrida MG,  Rosati S (2005) Development of recombinant chimeric antigen expressing immunodominant B epitopes of Leishmania infantum for serodiagnosis of visceral leishmaniasis.Clin Diagn Lab Immunol 12:647-653.
Boelaert M, El-Safi S, Hailu A, Mukhtar M, Rijal S, Sundar S, Wasunna M, Aseffa A, Mbui J, Menten J, Desjeux P,  Peeling RW (2008) Diagnostic tests for kala-azar: a multi-centre study of the freeze-dried DAT, rK39 strip test and KAtex in East Africa and the Indian subcontinent.Trans R Soc Trop Med Hyg 102:32-40.
Boelaert M, Rijal S, Regmi S, Singh R, Karki B, Jacquet D, Chappuis F, Campino L, Desjeux P, Le Ray D, Koirala S,  Van der Stuyft P (2004) A comparative study of the effectiveness of diagnostic tests for visceral leishmaniasis.Am J Trop Med Hyg 70:72-77.
Bray RS (1974) Leishmania.Annu Rev Microbiol 28:189-217.
Braz RF, Nascimento ET, Martins DR, Wilson ME, Pearson RD, Reed SG,  Jeronimo SM (2002) The sensitivity and specificity of Leishmania chagasi recombinant K39 antigen in the diagnosis of American visceral leishmaniasis and in differentiating active from subclinical infection.Am J Trop Med Hyg 67:344-348.
Burchmore RJ,  Barrett MP (2001) Life in vacuoles--nutrient acquisition by Leishmania amastigotes.Int J Parasitol 31:1311-1320.
Burki T (2009) East African countries struggle with visceral leishmaniasis.Lancet 374:371-372.
Calvopina M, Armijos RX,  Hashiguchi Y (2004) Epidemiology of leishmaniasis in Ecuador: current status of knowledge -- a review.Mem Inst Oswaldo Cruz 99:663-672.
Canavate C, Herrero M, Nieto J, Cruz I, Chicharro C, Aparicio P, Mulugeta A, Argaw D, Blackstock AJ, Alvar J,  Bern C (2011) Evaluation of two rK39 dipstick tests, direct agglutination test, and indirect fluorescent antibody test for diagnosis of visceral leishmaniasis in a new epidemic site in highland Ethiopia.Am J Trop Med Hyg 84:102-106.
Carvalho SF, Lemos EM, Corey R,  Dietze R (2003) Performance of recombinant K39 antigen in the diagnosis of Brazilian visceral leishmaniasis.Am J Trop Med Hyg 68:321-324.
Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, Alvar J,  Boelaert M (2007) Visceral leishmaniasis: what are the needs for diagnosis, treatment and control?Nat Rev Microbiol 5:873-882.
Collin S, Davidson R, Ritmeijer K, Keus K, Melaku Y, Kipngetich S,  Davies C (2004) Conflict and kala-azar: determinants of adverse outcomes of kala-azar among patients in southern Sudan.Clin Infect Dis 38:612-619.
Collin SM, Coleman PG, Ritmeijer K,  Davidson RN (2006) Unseen Kala-azar deaths in south Sudan (1999-2002).Trop Med Int Health 11:509-512.
Costa CH, Stewart JM, Gomes RB, Garcez LM, Ramos PK, Bozza M, Satoskar A, Dissanayake S, Santos RS, Silva MR, Shaw JJ, David JR,  Maguire JH (2002) Asymptomatic human carriers of Leishmania chagasi.Am J Trop Med Hyg 66:334-337.
Cupolillo E, Brahim LR, Toaldo CB, de Oliveira-Neto MP, de Brito ME, Falqueto A, de Farias Naiff M,  Grimaldi G, Jr. (2003) Genetic polymorphism and molecular epidemiology of Leishmania (Viannia) braziliensis from different hosts and geographic areas in Brazil.J Clin Microbiol 41:3126-3132.
Das BB, Ganguly A,  Majumder HK (2008) DNA topoisomerases of Leishmania: the potential targets for anti-leishmanial therapy.Adv Exp Med Biol 625:103-115.
De Doncker S, Hutse V, Abdellati S, Rijal S, Singh Karki BM, Decuypere S, Jacquet D, Le Ray D, Boelaert M, Koirala S,  Dujardin JC (2005) A new PCR-ELISA for diagnosis of visceral leishmaniasis in blood of HIV-negative subjects.Trans R Soc Trop Med Hyg 99:25-31.
Deborggraeve S, Laurent T, Espinosa D, Van der Auwera G, Mbuchi M, Wasunna M, El-Safi S, Al-Basheer AA, Arevalo J, Miranda-Verastegui C, Leclipteux T, Mertens P, Dujardin JC, Herdewijn P,  Buscher P (2008) A simplified and standardized polymerase chain reaction format for the diagnosis of leishmaniasis.J Infect Dis 198:1565-1572.
Dereure J, Rioux JA, Gallego M, Perieres J, Pratlong F, Mahjour J,  Saddiki H (1991a) Leishmania tropica in Morocco: infection in dogs.Trans R Soc Trop Med Hyg 85:595.
Dereure J, Rioux JA, Khiami A, Pratlong F, Perieres J,  Martini A (1991b) [Ecoepidemiology of leishmaniases in Syria. 2--Presence, in dogs, of Leishmania infantum Nicolle and Leishmania tropica (Wright) (Kinetoplastida-Trypanonomatidae)].Ann Parasitol Hum Comp 66:252-255.
Desjeux P (2004) Leishmaniasis: current situation and new perspectives.Comp Immunol Microbiol Infect Dis 27:305-318.
Desjeux P (2011) Kala Azar in South Asia: Current Status and Challenges Ahead.Springer Science + Business Media B.V. 111–124.
Dey A,  Singh S (2007) Genetic heterogeneity among visceral and post-Kala-Azar dermal leishmaniasis strains from eastern India.Infect Genet Evol 7:219-222.
Disch J, Pedras MJ, Orsini M, Pirmez C, de Oliveira MC, Castro M,  Rabello A (2005) Leishmania (Viannia) subgenus kDNA amplification for the diagnosis of mucosal leishmaniasis.Diagn Microbiol Infect Dis 51:185-190.
Dostalova A,  Volf P (2012) Leishmania development in sand flies: parasite-vector interactions overview.Parasit Vectors 5:276.
Dujardin JC (2006) Risk factors in the spread of leishmaniases: towards integrated monitoring?Trends Parasitol 22:4-6.
Evans TG, Teixeira MJ, McAuliffe IT, Vasconcelos I, Vasconcelos AW, Sousa Ade A, Lima JW,  Pearson RD (1992) Epidemiology of visceral leishmaniasis in northeast Brazil.J Infect Dis 166:1124-1132.
Faber WR, Oskam L, van Gool T, Kroon NC, Knegt-Junk KJ, Hofwegen H, van der Wal AC,  Kager PA (2003) Value of diagnostic techniques for cutaneous leishmaniasis.J Am Acad Dermatol 49:70-74.
Feasey N, Wansbrough-Jones M, Mabey DC,  Solomon AW (2010) Neglected tropical diseases.Br Med Bull 93:179-200.
Gadisa E, Custodio E, Canavate C, Sordo L, Abebe Z, Nieto J, Chicharro C, Aseffa A, Yamuah L, Engers H, Moreno J,  Cruz I (2012) Usefulness of the rK39-immunochromatographic test, direct agglutination test, and leishmanin skin test for detecting asymptomatic Leishmania infection in children in a new visceral leishmaniasis focus in Amhara State, Ethiopia.Am J Trop Med Hyg 86:792-798.
Gidwani K, Rai M, Chakravarty J, Boelaert M,  Sundar S (2009) Evaluation of leishmanin skin test in Indian visceral leishmaniasis.Am J Trop Med Hyg 80:566-567.
Hailu A, Gramiccia M,  Kager PA (2009) Visceral leishmaniasis in Aba-Roba, south-western Ethiopia: prevalence and incidence of active and subclinical infections.Ann Trop Med Parasitol 103:659-670.
Hailu A, Schoone GJ, Diro E, Tesfaye A, Techane Y, Tefera T, Assefa Y, Genetu A, Kebede Y, Kebede T,  Schallig HD (2006) Field evaluation of a fast anti-Leishmania antibody detection assay in Ethiopia.Trans R Soc Trop Med Hyg 100:48-52.
Handman E,  Bullen DV (2002) Interaction of Leishmania with the host macrophage.Trends Parasitol 18:332-334.
Herrero M, Orfanos G, Argaw D, Mulugeta A, Aparicio P, Parreno F, Bernal O, Rubens D, Pedraza J, Lima MA, Flevaud L, Palma PP, Bashaye S, Alvar J,  Bern C (2009) Natural history of a visceral leishmaniasis outbreak in highland Ethiopia.Am J Trop Med Hyg 81:373-377.
Herwaldt BL (1999) Leishmaniasis.Lancet 354:1191-1199.
Hommel M, Attar Z, Fargeas C, Dourado C, Monsigny M, Mayer R,  Chance ML (1997) The direct agglutination test: a non-specific test specific for the diagnosis of visceral leishmaniasis?Ann Trop Med Parasitol 91:795-802.
Hotez PJ, Remme JH, Buss P, Alleyne G, Morel C,  Breman JG (2004) Combating tropical infectious diseases: report of the Disease Control Priorities in Developing Countries Project.Clin Infect Dis 38:871-878.
Houghton RL, Petrescu M, Benson DR, Skeiky YA, Scalone A, Badaro R, Reed SG,  Gradoni L (1998) A cloned antigen (recombinant K39) of Leishmania chagasi diagnostic for visceral leishmaniasis in human immunodeficiency virus type 1 patients and a prognostic indicator for monitoring patients undergoing drug therapy.J Infect Dis 177:1339-1344.
Islam MZ, Itoh M, Mirza R, Ahmed I, Ekram AR, Sarder AH, Shamsuzzaman SM, Hashiguchi Y,  Kimura E (2004) Direct agglutination test with urine samples for the diagnosis of visceral leishmaniasis.Am J Trop Med Hyg 70:78-82.
Jacquet D, Boelaert M, Seaman J, Rijal S, Sundar S, Menten J,  Magnus E (2006) Comparative evaluation of freeze-dried and liquid antigens in the direct agglutination test for serodiagnosis of visceral leishmaniasis (ITMA-DAT/VL).Trop Med Int Health 11:1777-1784.
Jensen AT, Gaafar A, Ismail A, Christensen CB, Kemp M, Hassan AM, Kharazmi A,  Theander TG (1996) Serodiagnosis of cutaneous leishmaniasis: assessment of an enzyme-linked immunosorbent assay using a peptide sequence from gene B protein.Am J Trop Med Hyg 55:490-495.
Junqueira Pedras M, Orsini M, Castro M, Passos VM,  Rabello A (2003) Antibody subclass profile against Leishmania braziliensis and Leishmania amazonensis in the diagnosis and follow-up of mucosal leishmaniasis.Diagn Microbiol Infect Dis 47:477-485.
Kar K (1995) Serodiagnosis of leishmaniasis.Crit Rev Microbiol 21:123-152.
Khalil EA, Ayed NB, Musa AM, Ibrahim ME, Mukhtar MM, Zijlstra EE, Elhassan IM, Smith PG, Kieny PM, Ghalib HW, Zicker F, Modabber F,  Elhassan AM (2005) Dichotomy of protective cellular immune responses to human visceral leishmaniasis.Clin Exp Immunol 140:349-353.
Konecny P,  Stark DJ (2007) An Australian case of New World cutaneous leishmaniasis.Med J Aust 186:315-317.
Kuhls K, Keilonat L, Ochsenreither S, Schaar M, Schweynoch C, Presber W,  Schonian G (2007) Multilocus microsatellite typing (MLMT) reveals genetically isolated populations between and within the main endemic regions of visceral leishmaniasis.Microbes Infect 9:334-343.
Kumar P, Pai K, Tripathi K, Pandey HP,  Sundar S (2002) Immunoblot analysis of the humoral immune response to Leishmania donovani polypeptides in cases of human visceral leishmaniasis: its usefulness in prognosis.Clin Diagn Lab Immunol 9:1119-1123.
Kumar R, Kumar P, Chowdhary RK, Pai K, Mishra CP, Kumar K, Pandey HP, Singh VP,  Sundar S (1999) Kala-azar epidemic in Varanasi district, India.Bull World Health Organ 77:371-374.
Kumar R, Pai K, Pathak K,  Sundar S (2001) Enzyme-linked immunosorbent assay for recombinant K39 antigen in diagnosis and prognosis of Indian visceral leishmaniasis.Clin Diagn Lab Immunol 8:1220-1224.
Kumar S,  Tarleton RL (2001) Antigen-specific Th1 but not Th2 cells provide protection from lethal Trypanosoma cruzi infection in mice.J Immunol 166:4596-4603.
Maalej IA, Chenik M, Louzir H, Ben Salah A, Bahloul C, Amri F,  Dellagi K (2003) Comparative evaluation of ELISAs based on ten recombinant or purified Leishmania antigens for the serodiagnosis of Mediterranean visceral leishmaniasis.Am J Trop Med Hyg 68:312-320.
Machado de Assis TS, Rabello A,  Werneck GL (2012) Predictive models for the diagnostic of human visceral leishmaniasis in Brazil.PLoS Negl Trop Dis 6:e1542.
Markle WH,  Makhoul K (2004) Cutaneous leishmaniasis: recognition and treatment.Am Fam Physician 69:1455-1460.
Marsden PD,  Lumsden WH (1971) Trypanosomiasis and leishmaniasis.Practitioner 207:181-185.
Mary C, Faraut F, Lascombe L,  Dumon H (2004) Quantification of Leishmania infantum DNA by a real-time PCR assay with high sensitivity.J Clin Microbiol 42:5249-5255.
Mauricio IL, Stothard JR,  Miles MA (2000) The strange case of Leishmania chagasi.Parasitol Today 16:188-189.
Mauricio IL, Stothard JR,  Miles MA (2004) Leishmania donovani complex: genotyping with the ribosomal internal transcribed spacer and the mini-exon.Parasitology 128:263-267.
Maurya R, Singh RK, Kumar B, Salotra P, Rai M,  Sundar S (2005) Evaluation of PCR for diagnosis of Indian kala-azar and assessment of cure.J Clin Microbiol 43:3038-3041.
Mohebali M, Taran M,  Zarei Z (2004) Rapid detection of Leishmania infantum infection in dogs: comparative study using an immunochromatographic dipstick rk39 test and direct agglutination.Vet Parasitol 121:239-245.
Mosleh IM, Saliba EK, al-Khateeb MS, Bisharat Z, Oumeish OY,  Bitar W (1995) Serodiagnosis of cutaneous leishmaniasis in Jordan using indirect fluorescent antibody test and the enzyme-linked immunosorbent assay.Acta Trop 59:163-172.
Murray HW, Berman JD, Davies CR,  Saravia NG (2005) Advances in leishmaniasis.Lancet 366:1561-1577.
Murray HW, Pepin J, Nutman TB, Hoffman SL,  Mahmoud AA (2000) Tropical medicine.BMJ 320:490-494.
Osman OF, Oskam L, Kroon NC, Schoone GJ, Khalil ET, El-Hassan AM, Zijlstra EE,  Kager PA (1998) Use of PCR for diagnosis of post-kala-azar dermal leishmaniasis.J Clin Microbiol 36:1621-1624.
Osman OF, Oskam L, Zijlstra EE, Kroon NC, Schoone GJ, Khalil ET, El-Hassan AM,  Kager PA (1997) Evaluation of PCR for diagnosis of visceral leishmaniasis.J Clin Microbiol 35:2454-2457.
Pastor-Santiago JA, Chavez-Lopez S, Guzman-Bracho C, Flisser A,  Olivo-Diaz A (2012) American visceral leishmaniasis in Chiapas, Mexico.Am J Trop Med Hyg 86:108-114.
Pink R, Hudson A, Mouries MA,  Bendig M (2005) Opportunities and challenges in antiparasitic drug discovery.Nat Rev Drug Discov 4:727-740.
Pratt DM,  David JR (1981) Monoclonal antibodies that distinguish between New World species of Leishmania.Nature 291:581-583.
Quispe Tintaya KW, Ying X, Dedet JP, Rijal S, De Bolle X,  Dujardin JC (2004) Antigen genes for molecular epidemiology of leishmaniasis: polymorphism of cysteine proteinase B and surface metalloprotease glycoprotein 63 in the Leishmania donovani complex.J Infect Dis 189:1035-1043.
Ravindran R, Anam K, Bairagi BC, Saha B, Pramanik N, Guha SK, Goswami RP, Banerjee D,  Ali N (2004) Characterization of immunoglobulin G and its subclass response to Indian kala-azar infection before and after chemotherapy.Infect Immun 72:863-870.
Reithinger R, Dujardin JC, Louzir H, Pirmez C, Alexander B,  Brooker S (2007) Cutaneous leishmaniasis.Lancet Infect Dis 7:581-596.
Reithinger R, Quinnell RJ, Alexander B,  Davies CR (2002) Rapid detection of Leishmania infantum infection in dogs: comparative study using an immunochromatographic dipstick test, enzyme-linked immunosorbent assay, and PCR.J Clin Microbiol 40:2352-2356.
Rey LC, Martins CV, Ribeiro HB,  Lima AA (2005) American visceral leishmaniasis (kala-azar) in hospitalized children from an endemic area.J Pediatr (Rio J) 81:73-78.
Riera C, Fisa R, Lopez-Chejade P, Serra T, Girona E, Jimenez M, Muncunill J, Sedeno M, Mascaro M, Udina M, Gallego M, Carrio J, Forteza A,  Portus M (2008) Asymptomatic infection by Leishmania infantum in blood donors from the Balearic Islands (Spain).Transfusion 48:1383-1389.
Riera C, Fisa R, Lopez P, Ribera E, Carrio J, Falco V, Molina I, Gallego M,  Portus M (2004a) Evaluation of a latex agglutination test (KAtex) for detection of Leishmania antigen in urine of patients with HIV-Leishmania coinfection: value in diagnosis and post-treatment follow-up.Eur J Clin Microbiol Infect Dis 23:899-904.
Riera C, Fisa R, Udina M, Gallego M,  Portus M (2004b) Detection of Leishmania infantum cryptic infection in asymptomatic blood donors living in an endemic area (Eivissa, Balearic Islands, Spain) by different diagnostic methods.Trans R Soc Trop Med Hyg 98:102-110.
Rogers ME, Ilg T, Nikolaev AV, Ferguson MA,  Bates PA (2004) Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG.Nature 430:463-467.
Rosati S, Ortoffi M, Profiti M, Mannelli A, Mignone W, Bollo E,  Gradoni L (2003) Prokaryotic expression and antigenic characterization of three recombinant Leishmania antigens for serological diagnosis of canine leishmaniasis.Clin Diagn Lab Immunol 10:1153-1156.
Rosbotham JL, Corbett EL, Grant HR, Hay RJ,  Bryceson AD (1996) Imported mucocutaneous leishmaniasis.Clin Exp Dermatol 21:288-290.
Ryan L, Vexenat A, Marsden PD, Lainson R,  Shaw JJ (1990) The importance of rapid diagnosis of new cases of cutaneous leishmaniasis in pin-pointing the sandfly vector.Trans R Soc Trop Med Hyg 84:786.
Salotra P,  Singh R (2006) Challenges in the diagnosis of post kala-azar dermal leishmaniasis.Indian J Med Res 123:295-310.
Salotra P, Sreenivas G, Beena KR, Mukherjee A,  Ramesh V (2003) Parasite detection in patients with post kala-azar dermal leishmaniasis in India: a comparison between molecular and immunological methods.J Clin Pathol 56:840-843.
Salotra P, Sreenivas G, Pogue GP, Lee N, Nakhasi HL, Ramesh V,  Negi NS (2001) Development of a species-specific PCR assay for detection of Leishmania donovani in clinical samples from patients with kala-azar and post-kala-azar dermal leishmaniasis.J Clin Microbiol 39:849-854.
Seaman J, Mercer AJ,  Sondorp E (1996) The epidemic of visceral leishmaniasis in western Upper Nile, southern Sudan: course and impact from 1984 to 1994.Int J Epidemiol 25:862-871.
Seifert K, Perez-Victoria FJ, Stettler M, Sanchez-Canete MP, Castanys S, Gamarro F,  Croft SL (2007) Inactivation of the miltefosine transporter, LdMT, causes miltefosine resistance that is conferred to the amastigote stage of Leishmania donovani and persists in vivo.Int J Antimicrob Agents 30:229-235.
Sharma NL, Mahajan VK, Kanga A, Sood A, Katoch VM, Mauricio I, Singh CD, Parwan UC, Sharma VK,  Sharma RC (2005) Localized cutaneous leishmaniasis due to Leishmania donovani and Leishmania tropica: preliminary findings of the study of 161 new cases from a new endemic focus in himachal pradesh, India.Am J Trop Med Hyg 72:819-824.
Siddig M, Ghalib H, Shillington DC,  Petersen EA (1988) Visceral leishmaniasis in the Sudan: comparative parasitological methods of diagnosis.Trans R Soc Trop Med Hyg 82:66-68.
Silva ES, Schoone GJ, Gontijo CM, Brazil RP, Pacheco RS,  Schallig HD (2005) 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 Biol Dis 4:4.
Singh S, Kumari V,  Singh N (2002) Predicting kala-azar disease manifestations in asymptomatic patients with latent Leishmania donovani infection by detection of antibody against recombinant K39 antigen.Clin Diagn Lab Immunol 9:568-572.
Singh S,  Sivakumar R (2003) Recent advances in the diagnosis of leishmaniasis.J Postgrad Med 49:55-60.
Singh SP, Reddy DC, Rai M,  Sundar S (2006) Serious underreporting of visceral leishmaniasis through passive case reporting in Bihar, India.Trop Med Int Health 11:899-905.
Smyth AJ, Ghosh A, Hassan MQ, Basu D, De Bruijn MH, Adhya S, Mallik KK,  Barker DC (1992) Rapid and sensitive detection of Leishmania kinetoplast DNA from spleen and blood samples of kala-azar patients.Parasitology 105 ( Pt 2):183-192.
Sreenivas G, Ansari NA, Singh R, Subba Raju BV, Bhatheja R, Negi NS,  Salotra R (2002) Diagnosis of visceral leishmaniasis: comparative potential of amastigote antigen, recombinant antigen and PCR.Br J Biomed Sci 59:218-222.
Srivastava P, Dayama A, Mehrotra S,  Sundar S (2011a) Diagnosis of visceral leishmaniasis.Trans R Soc Trop Med Hyg 105:1-6.
Srivastava P, Mehrotra S, Tiwary P, Chakravarty J,  Sundar S (2011b) Diagnosis of Indian visceral leishmaniasis by nucleic acid detection using PCR.PLoS One 6:e19304.
Srividya G, Kulshrestha A, Singh R,  Salotra P (2012) Diagnosis of visceral leishmaniasis: developments over the last decade.Parasitol Res 110:1065-1078.
Sundar S, Agrawal S, Pai K, Chance M,  Hommel M (2005) Detection of leishmanial antigen in the urine of patients with visceral leishmaniasis by a latex agglutination test.Am J Trop Med Hyg 73:269-271.
Sundar S, Singh RK, Maurya R, Kumar B, Chhabra A, Singh V,  Rai M (2006) Serological diagnosis of Indian visceral leishmaniasis: direct agglutination test versus rK39 strip test.Trans R Soc Trop Med Hyg 100:533-537.
Topno RK, Das VN, Ranjan A, Pandey K, Singh D, Kumar N, Siddiqui NA, Singh VP, Kesari S, Bimal S, Kumar AJ, Meena C, Kumar R,  Das P (2010) Asymptomatic infection with visceral leishmaniasis in a disease-endemic area in bihar, India.Am J Trop Med Hyg 83:502-506.
van den Bogaart E, Berkhout MM, Adams ER, Mens PF, Sentongo E, Mbulamberi DB, Straetemans M, Schallig HD,  Chappuis F (2012) Prevalence, features and risk factors for malaria co-infections amongst visceral leishmaniasis patients from Amudat Hospital, Uganda.PLoS Negl Trop Dis 6:e1617.
van den Bogaart E, Berkhout MM, Nour AB, Mens PF, Talha AB, Adams ER, Ahmed HB, Abdelrahman SH, Ritmeijer K, Nour BY,  Schallig HD (2013) Concomitant malaria among visceral leishmaniasis in-patients from Gedarif and Sennar States, Sudan: a retrospective case-control study.BMC Public Health 13:332.
Vega-Lopez F (2003) Diagnosis of cutaneous leishmaniasis.Curr Opin Infect Dis 16:97-101.
Weigle KA, Labrada LA, Lozano C, Santrich C,  Barker DC (2002) PCR-based diagnosis of acute and chronic cutaneous leishmaniasis caused by Leishmania (Viannia).J Clin Microbiol 40:601-606.
Werneck GL, Batista MS, Gomes JR, Costa DL,  Costa CH (2003) Prognostic factors for death from visceral leishmaniasis in Teresina, Brazil.Infection 31:174-177.
WHO
WHO. (1990) Control of the Leishmaniasis. Technical Report. ;(Series 793).
WHO. (2002) The world health report—reducing risks, promoting healthy life. Geneva, Switzerland: World Health Organization.
WHO. (2007) Leishmaniasis Control. http://www.who.int/topics/leishmaniasis/en/.
Yahia H, Ready PD, Hamdani A, Testa JM,  Guessous-Idrissi N (2004) Regional genetic differentiation of Phlebotomus sergenti in three Moroccan foci of cutaneous leishmaniasis caused by Leishmania tropica.Parasite 11:189-199.
Yamey G,  Torreele E (2002) The world's most neglected diseases.BMJ 325:176-177.
Zijlstra EE, Daifalla NS, Kager PA, Khalil EA, El-Hassan AM, Reed SG,  Ghalib HW (1998) rK39 enzyme-linked immunosorbent assay for diagnosis of Leishmania donovani infection.Clin Diagn Lab Immunol 5:717-720.
Zijlstra EE,  el-Hassan AM (2001) Leishmaniasis in Sudan. Visceral leishmaniasis.Trans R Soc Trop Med Hyg 95 Suppl 1:S27-58.
Zijlstra EE, el-Hassan AM, Ismael A,  Ghalib HW (1994) Endemic kala-azar in eastern Sudan: a longitudinal study on the incidence of clinical and subclinical infection and post-kala-azar dermal leishmaniasis.Am J Trop Med Hyg 51:826-836.
Zijlstra EE, Khalil EA, Kager PA,  El-Hassan AM (2000) Post-kala-azar dermal leishmaniasis in the Sudan: clinical presentation and differential diagnosis.Br J Dermatol 143:136-143.
Zijlstra EE, Musa AM, Khalil EA, el-Hassan IM,  el-Hassan AM (2003) Post-kala-azar dermal leishmaniasis.Lancet Infect Dis 3:87-98.
The HIV-VL co-infection is characterized by a high fatality rate and frequent relapses, and cases play an important infectious reservoir (Alvar et al. 2008).
L. tropica was considered to be a strict anthroponosis, but several cases of canine infection have been described (Dereure et al. 1991a; Dereure et al. 1991b; Yahia et al. 2004).