Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-22T18:04:03.721Z Has data issue: false hasContentIssue false
  • English
  • Français

Implications of co-infection of Leptomonas in visceral leishmaniasis in India

Published online by Cambridge University Press:  23 October 2015

ANGAMUTHU SELVAPANDIYAN ,
KAVITA AHUJA ,
NITI PURI  and
ANUJA KRISHNAN
ANGAMUTHU SELVAPANDIYAN*
Affiliation:
Infectious Diseases, Institute of Molecular Medicine, New Delhi, 110020, India Department of Research, Sir Gangaram Hospital, New Delhi, 110060, India
KAVITA AHUJA
Affiliation:
Infectious Diseases, Institute of Molecular Medicine, New Delhi, 110020, India Department of Bio and Nano Technology, Guru Jambheshwar University of Science and Technology, Hisar 125001, Haryana, India
NITI PURI
Affiliation:
The School of Life Sciences, Jawaharlal Nehru University, New Delhi, 110067, India
ANUJA KRISHNAN
Affiliation:
Infectious Diseases, Institute of Molecular Medicine, New Delhi, 110020, India
*
* Corresponding author: Infectious Diseases, Institute of Molecular Medicine, New Delhi, 110020, India. E-mail: selvapandiyan@immindia.org
Get access Rights & Permissions [Opens in a new window]

Summary

Protozoan parasites Leishmania donovani (family: Trypanosomatidae) cause fatal visceral leishmaniasis (VL) and the infection relapses in apparently cured population as post kala-azar dermal leishmaniasis (PKDL) in the Indian subcontinent. In recent years co-infection of another Trypanosomatid parasite Leptomonas with L. donovani during VL/PKDL in this region has become prominent. The observation of clinically lesser-known insect parasite, Leptomonas in leishmaniasis is intriguing to researchers. The presence of Leishmania look alike Leptomonas in the cultures of clinical isolates of Leishmania has been worrisome to those, who prefer to work with pure Leishmania cultures for drug and vaccine development or immune response studies. The exact implications of such a co-habitation, which might lead to a delay in the diagnostics of VL and elevate mortality, need a thorough investigation. Also whether Leptomonas is involved in leishmaniasis manifestation needs to be ascertained. Thus we are currently witnessing a new paradigm of a parasitic co-infection in VL/PKDL cases in India and this review outlines various opportunities for further research in understanding such emerging co-infection.

Keywords

LeishmaniaLeptomonasco-infectionvisceral leishmaniasispost kala-azar leishmaniasissandfly
Type
Review Article
Information
Parasitology , Volume 142 , Issue 14 , December 2015 , pp. 1657 - 1662
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

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

Ahuja, K., Arora, G., Khare, P. and Selvapandiyan, A. (2015). Selective elimination of Leptomonas from the in vitro co-culture with Leishmania. Parasitology International 64, 1–5.CrossRefGoogle ScholarPubMed
Alvar, J., Velez, I. D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J., den Boer, M. and Team, W. H. O. L. C. (2012). Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7, e35671.CrossRefGoogle ScholarPubMed
Bacchi, C. J., Lambros, C., Ellenbogen, B. B., Penkovsky, L. N., Sullivan, W., Eyinna, E. E. and Hutner, S. H. (1975). Drug-resistant Leptomonas: cross-resistance in trypanocide-resistant clones. Antimicrobial Agents and Chemotherapy 8, 688–692.CrossRefGoogle ScholarPubMed
Bacchi, J., Lambros, C., Goldberg, B., Hutner, S. H. and de Carvalho, G. D. (1974). Susceptibility of an insect Leptomonas and Crithidia fasciculata to several established antitrypanosomatid agents. Antimicrobial Agents and Chemotherapy 6, 785–790.CrossRefGoogle ScholarPubMed
Bellofatto, V., Torres-Munoz, J. E. and Cross, G. A. (1991). Stable transformation of Leptomonas seymouri by circular extrachromosomal elements. Proceedings of the National Academy of Sciences of the United States of America 88, 6711–6715.CrossRefGoogle ScholarPubMed
Bhattarai, N. R., Das, M. L., Rijal, S., van der Auwera, G., Picado, A., Khanal, B., Roy, L., Speybroeck, N., Berkvens, D., Davies, C. R., Coosemans, M., Boelaert, M. and Dujardin, J. C. (2009). Natural infection of Phlebotomus argentipes with Leishmania and other trypanosomatids in a visceral leishmaniasis endemic region of Nepal. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 1087–1092.CrossRefGoogle Scholar
Braga, A. R., Correa, A. P., Camossi, L. G., Silva, R. C., Langoni, H. and Lucheis, S. B. (2014). Coinfection by Toxoplasma gondii and Leishmania spp. in domestic cats (Felis catus) in State of Mato Grosso do Sul. Revista da Sociedade Brasileira de Medicina Tropical 47, 796–797.CrossRefGoogle ScholarPubMed
Cota, G. F., Gomes, L. I., Pinto, B. F., Santos-Oliveira, J. R., Da-Cruz, A. M., Pedrosa, M. S., Tafuri, W. L. and Rabello, A. (2012). Dyarrheal syndrome in a patient co-infected with Leishmania infantum and Schistosoma mansoni . Case Reports in Medicine 2012, 240512.CrossRefGoogle Scholar
da Silva, R. C., Caffaro, K., Paula, C. L., Risseti, R. M., Langoni, H., Megid, J., Melanchauski, M. S., Souza, K. L., Takahira, R. K. and Machado, V. M. (2015). An atypical Toxoplasma gondii genotype in a rural Brazilian dog co-infected with Leishmania (Viannia) braziliensis. Revista da Sociedade Brasileira de Medicina Tropical 48, 224–227.CrossRefGoogle Scholar
Dedet, J. P., Roche, B., Pratlong, F., Cales-Quist, D., Jouannelle, J., Benichou, J. C. and Huerre, M. (1995). Diffuse cutaneous infection caused by a presumed monoxenous trypanosomatid in a patient infected with HIV. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 644–646.CrossRefGoogle Scholar
Diro, E., Lynen, L., Ritmeijer, K., Boelaert, M., Hailu, A. and van Griensven, J. (2014). Visceral Leishmaniasis and HIV coinfection in East Africa. PLoS Neglected Tropical Diseases 8, e2869.CrossRefGoogle ScholarPubMed
Ferreira, L. R., Kesper, N., Teixeira, M. M., Laurenti, M. D., Barbieri, C. L., Lindoso, J. A. and Umezawa, E. S. (2014). New insights about cross-reactive epitopes of six trypanosomatid genera revealed that Crithidia and Leptomonas have antigenic similarity to L. (L.) chagasi. Acta Tropica 131, 41–46.CrossRefGoogle Scholar
Ganguly, S., Das, N. K., Barbhuiya, J. N. and Chatterjee, M. (2010). Post-kala-azar dermal leishmaniasis--an overview. International Journal of Dermatology 49, 921–931.CrossRefGoogle ScholarPubMed
Ghosh, S., Banerjee, P., Sarkar, A., Datta, S. and Chatterjee, M. (2012). Coinfection of Leptomonas seymouri and Leishmania donovani in Indian leishmaniasis. Journal of Clinical Microbiology 50, 2774–2778.CrossRefGoogle ScholarPubMed
Gil, J., Cimino, R., Lopez Quiroga, I., Cajal, S., Acosta, N., Juarez, M., Zacca, R., Orellana, V., Krolewiecki, A., Diosque, P. and Nasser, J. (2011). [Reactivity of GST-SAPA antigen of Trypanosoma cruzi against sera from patients with Chagas disease and leishmaniasis]. Medicina (B Aires) 71, 113–119.Google ScholarPubMed
Goldberg, B., Lambros, C., Bacchi, C. J. and Hutner, S. H. (1974). Inhibition by several standard antiprotozoal drugs of growth and O2 uptake of cells and particulate preparations of a Leptomonas. Journal of Protozoology 21, 322–326.CrossRefGoogle ScholarPubMed
Griemberg, G., Ferrarotti, N. F., Svibel, G., Ravelli, M. R., Taranto, N. J., Malchiodi, E. L. and Pizzimenti, M. C. (2006). [Immunofluorescence assay with Crithidia luciliae for the detection of anti-DNA antibodies. Atypical images and their relationship with Chagas’ disease and leishmaniasis]. Medicina (B Aires) 66, 3–8.Google ScholarPubMed
Jain, K. and Jain, N. K. (2015). Vaccines for visceral leishmaniasis: a review. Journal of Immunology and Methods 422, 1–12.CrossRefGoogle ScholarPubMed
Jimenez, M. I., Lopez-Velez, R., Molina, R., Canavate, C. and Alvar, J. (1996). HIV co-infection with a currently non-pathogenic flagellate. Lancet 347, 264–265.CrossRefGoogle ScholarPubMed
Johnson, P., Neal, R. A. and Gall, D. (1963). Protective effect of killed Trypanosome vaccines with incorporated adjuvants. Nature 200, 83.CrossRefGoogle ScholarPubMed
Kedzierski, L. and Evans, K. J. (2014). Immune responses during cutaneous and visceral leishmaniasis. Parasitology 141, 1544–1562.CrossRefGoogle Scholar
Kraeva, N., Butenko, A., Hlavacova, J., Kostygov, A., Myskova, J., Grybchuk, D., Lestinova, T., Votypka, J., Volf, P., Opperdoes, F., Flegontov, P., Lukes, J. and Yurchenko, V. (2015). Leptomonas seymouri: adaptations to the dixenous life cycle analyzed by genome sequencing, transcriptome profiling and co-infection with Leishmania donovani . PLoS Pathogens 11, e1005127.CrossRefGoogle Scholar
Kumar, D., Ramesh, V., Verma, S., Ramam, M. and Salotra, P. (2009). Post-kala-azar dermal leishmaniasis (PKDL) developing after treatment of visceral leishmaniasis with amphotericin B and miltefosine. Annals of Tropical Medicine and Parasitology 103, 727–730.CrossRefGoogle ScholarPubMed
Kutish, G. F. and Janovy, J. Jr. (1981). Inhibition of in vitro macrophage digestion capacity by infection with Leishmania donovani (Protozoa: Kinetoplastida). Journal of Parasitology 67, 457–462.CrossRefGoogle ScholarPubMed
Lukes, J., Skalicky, T., Tyc, J., Votypka, J. and Yurchenko, V. (2014). Evolution of parasitism in kinetoplastid flagellates. Molecular and Biochemical Parasitology 195, 115–122.CrossRefGoogle ScholarPubMed
McGhee, R. B. and Cosgrove, W. B. (1980). Biology and physiology of the lower Trypanosomatidae. Microbiological Reviews 44, 140–173.CrossRefGoogle ScholarPubMed
Medrano, F. J., Hernandez-Quero, J., Jimenez, E., Pineda, J. A., Rivero, A., Sanchez-Quijano, A., Velez, I. D., Viciana, P., Castillo, R. and Reyes, M. J. (1992). Visceral leishmaniasis in HIV-1-infected individuals: a common opportunistic infection in Spain? AIDS 6, 1499–1503.CrossRefGoogle ScholarPubMed
Moreira, D., Lopez-Garcia, P. and Vickerman, K. (2004). An updated view of kinetoplastid phylogeny using environmental sequences and a closer outgroup: proposal for a new classification of the class Kinetoplastea. International Journal of Systematic and Evolutionary Microbiology 54, 1861–1875.CrossRefGoogle Scholar
Morio, F., Reynes, J., Dollet, M., Pratlong, F., Dedet, J. P. and Ravel, C. (2008). Isolation of a protozoan parasite genetically related to the insect trypanosomatid Herpetomonas samuelpessoai from a human immunodeficiency virus-positive patient. Journal of Clinicial Microbiology 46, 3845–3847.CrossRefGoogle Scholar
Nylen, S. and Gautam, S. (2010). Immunological perspectives of leishmaniasis. Journal of Global Infectious Diseases 2, 135–146.CrossRefGoogle ScholarPubMed
Pacheco, R. S., Marzochi, M. C., Pires, M. Q., Brito, C. M., Madeira Mde, F. and Barbosa-Santos, E. G. (1998). Parasite genotypically related to a monoxenous trypanosomatid of dog's flea causing opportunistic infection in an HIV positive patient. Memorias do Instituto Oswaldo Cruz 93, 531–537.CrossRefGoogle Scholar
Patole, S., Burza, S. and Varghese, G. M. (2014). Multiple relapses of visceral leishmaniasis in a patient with HIV in India: a treatment challenge. International Journal of Infectious Diseases 25, 204–206.CrossRefGoogle Scholar
Rathnayake, D., Ranawake, R. R., Sirimanna, G., Siriwardhane, Y., Karunaweera, N. and De Silva, R. (2010). Co-infection of mucosal leishmaniasis and extra pulmonary tuberculosis in a patient with inherent immune deficiency. International Journal of Dermatology 49, 549–551.CrossRefGoogle Scholar
Selvapandiyan, A., Dey, R., Gannavaram, S., Lakhal-Naouar, I., Duncan, R., Salotra, P. and Nakhasi, H. L. (2012). Immunity to visceral leishmaniasis using genetically defined live-attenuated parasites. Journal of Tropical Medicine 2012, 631460.CrossRefGoogle ScholarPubMed
Selvapandiyan, A., Dey, R., Gannavaram, S., Solanki, S., Salotra, P. and Nakhasi, H. L. (2014). Generation of growth arrested Leishmania amastigotes: a tool to develop live attenuated vaccine candidates against visceral leishmaniasis. Vaccine 32, 3895–3901.CrossRefGoogle ScholarPubMed
Selvapandiyan, A., Dey, R., Nylen, S., Duncan, R., Sacks, D. and Nakhasi, H. L. (2009). Intracellular replication-deficient Leishmania donovani induces long lasting protective immunity against visceral leishmaniasis. Journal of Immunology 183, 1813–1820.CrossRefGoogle ScholarPubMed
Shah, S., Shah, A., Prajapati, S. and Bilimoria, F. (2010). Post-kala-azar dermal leishmaniasis in HIV-positive patients: a study of two cases. Indian Journal of Sexually Transmitted Diseases 31, 42–44.CrossRefGoogle ScholarPubMed
Singh, S. (2014). Changing trends in the epidemiology, clinical presentation, and diagnosis of Leishmania-HIV co-infection in India. International Journal of Infectious Diseases 29, 103–112.CrossRefGoogle ScholarPubMed
Singh, N., Chikara, S. and Sundar, S. (2013). SOLiD sequencing of genomes of clinical isolates of Leishmania donovani from India confirm leptomonas co-infection and raise some key questions. PLoS ONE 8, e55738.Google ScholarPubMed
Singh, R. K., Pandey, H. P. and Sundar, S. (2006). Visceral leishmaniasis (kala-azar): challenges ahead. Indian Journal of Medical Research 123, 331–344.Google ScholarPubMed
Souza Mdo, C., Reis, A. P., Da Silva, W. D. and Brener, Z. (1974). Mechanism of acquired immunity induced by “Leptomonas pessoai” against Trypanosoma cruzi in mice. Journal of Protozoology 21, 579–584.CrossRefGoogle ScholarPubMed
Srivastava, P., Prajapati, V. K., Vanaerschot, M., Van der Auwera, G., Dujardin, J. C. and Sundar, S. (2010). Detection of Leptomonas sp. parasites in clinical isolates of Kala-azar patients from India. Infection Genetics and Evolution 10, 1145–1150.CrossRefGoogle ScholarPubMed
Sundar, S. and Chatterjee, M. (2006). Visceral leishmaniasis – current therapeutic modalities. Indian Journal of Medical Research 123, 345–352.Google ScholarPubMed
Tyzzer, E. E. and Walker, E. L. (1919). A comparative study of Leishmania Infantum of Infantile Kala Azar and Leptomonas (Herpetomonas) Ctenocephali Parasitic in the gut of the Dog Flea. Journal of Medical Research 40, 129–176.Google ScholarPubMed
van den Bogaart, E., Berkhout, M. M., Nour, A. B., Mens, P. F., Talha, A. B., Adams, E. R., Ahmed, H. B., Abdelrahman, S. H., Ritmeijer, K., Nour, B. Y. and Schallig, H. D. (2013). Concomitant malaria among visceral leishmaniasis in-patients from Gedarif and Sennar States, Sudan: a retrospective case-control study. BMC Public Health 13, 332.CrossRefGoogle ScholarPubMed
van Griensven, J., Carrillo, E., Lopez-Velez, R., Lynen, L. and Moreno, J. (2014). Leishmaniasis in immunosuppressed individuals. Clinical Microbiology and Infection 20, 286–299.CrossRefGoogle ScholarPubMed
Vega Benedetti, A. F., Cimino, R. O., Cajal, P. S., Juarez Mdel, V., Villalpando, C. A., Gil, J. F., Marcipar, I. S., Krolewiecki, A. J. and Nasser, J. R. (2013). Performance of different Trypanosoma cruzi antigens in the diagnosis of Chagas disease in patients with American cutaneous leishmaniasis from a co-endemic region in Argentina. Tropical Medicine and International Health 18, 1103–1109.CrossRefGoogle ScholarPubMed
Weirather, J. L., Jeronimo, S. M., Gautam, S., Sundar, S., Kang, M., Kurtz, M. A., Haque, R., Schriefer, A., Talhari, S., Carvalho, E. M., Donelson, J. E. and Wilson, M. E. (2011). Serial quantitative PCR assay for detection, species discrimination, and quantification of Leishmania spp. in human samples. Journal of Clinical Microbiology 49, 3892–3904.CrossRefGoogle ScholarPubMed
Yurchenko, V. Y., Lukes, J., Jirku, M., Zeledon, R. and Maslov, D. A. (2006). Leptomonas costaricensis sp. n. (Kinetoplastea: Trypanosomatidae), a member of the novel phylogenetic group of insect trypanosomatids closely related to the genus Leishmania. Parasitology 133, 537–546.CrossRefGoogle Scholar