Genetic variation and geographic distribution of Leishmania orientalis and Leishmania martiniquensis among Leishmania/HIV co-infection in Thailand.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
28 Dec 2023
Historique:
received: 19 07 2023
accepted: 21 12 2023
medline: 29 12 2023
pubmed: 29 12 2023
entrez: 28 12 2023
Statut: epublish

Résumé

Since 1999, the number of asymptomatic leishmaniasis cases has increased continuously in Thailand, particularly among patients with HIV who are prone to develop symptoms of cutaneous and visceral leishmaniasis further. The asymptomatic infection could play a key role in Leishmania transmission and distribution. Understanding population structure and phylogeographic patterns could be crucially needed to develop effective diagnoses and appropriate guidelines for therapy. In this study, genetic variation and geographic distribution of the Leishmania/HIV co-infected population were investigated in endemic northern and southern Thailand. Interestingly, Leishmania orientalis was common and predominant in these two regions with common regional haplotype distribution but not for the others. Recent population expansion was estimated, probably due to the movement and migration of asymptomatic individuals; therefore, the transmission and prevalence of Leishmania infection could be underestimated. These findings of imbalanced population structure and phylogeographic distribution patterns provide valuable, insightful population structure and geographic distribution of Leishmania/HIV co-infection to empower prevention and control of transmission and expansion of asymptomatic leishmaniasis.

Identifiants

pubmed: 38155252
doi: 10.1038/s41598-023-50604-4
pii: 10.1038/s41598-023-50604-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

23094

Informations de copyright

© 2023. The Author(s).

Références

WHO. Global leishmaniasis update, 2006–2015: A turning point in leishmaniasis surveillance. Wkly. Epidemiol. Rec. 92, 557–565 (2017).
Maroli, M., Feliciangeli, M. D., Bichaud, L., Charrel, R. N. & Gradoni, L. Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med. Vet. Entomol. 27, 123–147. https://doi.org/10.1111/j.1365-2915.2012.01034.x (2013).
doi: 10.1111/j.1365-2915.2012.01034.x pubmed: 22924419
Steverding, D. The history of leishmaniasis. Parasites Vectors 10, 82. https://doi.org/10.1186/s13071-017-2028-5 (2017).
doi: 10.1186/s13071-017-2028-5 pubmed: 28202044 pmcid: 5312593
Manomat, J. et al. Prevalence and risk factors associated with Leishmania infection in Trang Province, southern Thailand. PLoS Negl. Trop. Dis. 11, e0006095. https://doi.org/10.1371/journal.pntd.0006095 (2017).
doi: 10.1371/journal.pntd.0006095 pubmed: 29155831 pmcid: 5714378
Srivarasat, S. et al. Case Report: Autochthonous disseminated cutaneous, mucocutaneous, and visceral leishmaniasis caused by Leishmania martiniquensis in a patient with HIV/AIDS from northern Thailand and literature review. Am. J. Trop. Med. Hyg. 107, 1196–1202. https://doi.org/10.4269/ajtmh.22-0108 (2022).
doi: 10.4269/ajtmh.22-0108 pubmed: 36375453 pmcid: 9768252
Lindoso, J. A., Cunha, M. A., Queiroz, I. T. & Moreira, C. H. Leishmaniasis-HIV co-infection: Current challenges. HIV AIDS (Auckl.) 8, 147–156. https://doi.org/10.2147/hiv.S93789 (2016).
doi: 10.2147/hiv.S93789 pubmed: 27785103
Leelayoova, S. et al. Leishmaniasis in Thailand: A review of causative agents and situations. Am. J. Trop. Med. Hyg. 96, 534–542. https://doi.org/10.4269/ajtmh.16-0604 (2017).
doi: 10.4269/ajtmh.16-0604 pubmed: 28093539 pmcid: 5361524
Thisyakorn, U., Jongwutiwes, S., Vanichsetakul, P. & Lertsapcharoen, P. Visceral leishmaniasis: the first indigenous case report in Thailand. Trans. R. Soc. Trop. Med. Hyg. 93, 23–24. https://doi.org/10.1016/S0035-9203(99)90166-9 (1999).
doi: 10.1016/S0035-9203(99)90166-9 pubmed: 10492782
Bualert, L. et al. Autochthonous disseminated dermal and visceral leishmaniasis in an AIDS patient, southern Thailand, caused by Leishmania siamensis. Am. J. Trop. Med. Hyg. 86, 821–824. https://doi.org/10.4269/ajtmh.2012.11-0707 (2012).
doi: 10.4269/ajtmh.2012.11-0707 pubmed: 22556080 pmcid: 3335686
Charyyeva, A. et al. Genetic diversity of Leishmania tropica: unexpectedly complex distribution pattern. Acta Trop. 218, 105888. https://doi.org/10.1016/j.actatropica.2021.105888 (2021).
doi: 10.1016/j.actatropica.2021.105888 pubmed: 33713626
Akopyants, N. S. et al. Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 324, 265–268. https://doi.org/10.1126/science.1169464 (2009).
doi: 10.1126/science.1169464 pubmed: 19359589 pmcid: 2729066
Chargui, N. et al. Population structure of Tunisian Leishmania infantum and evidence for the existence of hybrids and gene flow between genetically different populations. Int. J. Parasitol. 39, 801–811. https://doi.org/10.1016/j.ijpara.2008.11.016 (2009).
doi: 10.1016/j.ijpara.2008.11.016 pubmed: 19211023
Sills, J., Volf, P. & Sadlova, J. Sex in Leishmania. Science 324, 1644–1644. https://doi.org/10.1126/science.324_1644b (2009).
doi: 10.1126/science.324_1644b
Botilde, Y. et al. Comparison of molecular markers for strain typing of Leishmania infantum. Infect. Genet. Evol. 6, 440–446. https://doi.org/10.1016/j.meegid.2006.02.003 (2006).
doi: 10.1016/j.meegid.2006.02.003 pubmed: 16581311
Fotouhi-Ardakani, R. et al. Assessment of nuclear and mitochondrial genes in precise identification and analysis of genetic polymorphisms for the evaluation of Leishmania parasites. Infect. Genet. Evol. 46, 33–41. https://doi.org/10.1016/j.meegid.2016.10.011 (2016).
doi: 10.1016/j.meegid.2016.10.011 pubmed: 27765638
Ghatee, M. A. et al. Heterogeneity of the internal transcribed spacer region in Leishmania tropica isolates from southern Iran. Exp. Parasitol. 144, 44–51. https://doi.org/10.1016/j.exppara.2014.06.003 (2014).
doi: 10.1016/j.exppara.2014.06.003 pubmed: 24932536
Schönian, G., Cupolillo, E. & Mauricio, I. in Drug Resistance in Leishmania Parasites: Consequences, Molecular Mechanisms and Possible Treatments (eds. Alicia Ponte-Sucre, Emilia Diaz, & Maritza Padrón-Nieves) 15–44 (Springer Vienna, 2013).
Hitakarun, A. et al. Comparison of PCR methods for detection of Leishmania siamensis infection. Parasites Vectors 7, 458. https://doi.org/10.1186/s13071-014-0458-x (2014).
doi: 10.1186/s13071-014-0458-x pubmed: 25274259 pmcid: 4188918
Ruang-areerate, T. et al. Development of loop-mediated isothermal amplification (LAMP) assay using SYBR safe and gold-nanoparticle probe for detection of Leishmania in HIV patients. Sci. Rep. 11, 12152. https://doi.org/10.1038/s41598-021-91540-5 (2021).
doi: 10.1038/s41598-021-91540-5 pubmed: 34108543 pmcid: 8190085
Sukphattanaudomchoke, C. et al. Simplified closed tube loop mediated isothermal amplification (LAMP) assay for visual diagnosis of Leishmania infection. Acta Trop. 212, 105651. https://doi.org/10.1016/j.actatropica.2020.105651 (2020).
doi: 10.1016/j.actatropica.2020.105651 pubmed: 32763231
Thita, T., Manomat, J., Leelayoova, S., Mungthin, M. & Ruang-areerate, T. Reliable interpretation and long-term stability using SYBR™ safe fluorescent assay for loop-mediated isothermal amplification (LAMP) detection of Leishmania spp. Trop. Biomed. 36, 495–504 (2019).
pubmed: 33597412
Ruang-areerate, T. et al. Distance-based paper device using combined SYBR safe and gold nanoparticle probe LAMP assay to detect Leishmania among patients with HIV. Sci. Rep. 12, 14558. https://doi.org/10.1038/s41598-022-18765-w (2022).
doi: 10.1038/s41598-022-18765-w pubmed: 36028548 pmcid: 9418321
Jariyapan, N. et al. Leishmania (Mundinia) orientalis n. sp. (Trypanosomatidae), a parasite from Thailand responsible for localised cutaneous leishmaniasis. Parasites Vectors 11, 351. https://doi.org/10.1186/s13071-018-2908-3 (2018).
doi: 10.1186/s13071-018-2908-3 pubmed: 29914526 pmcid: 6006788
Sriwongpan, P. et al. Prevalence and associated risk factors of Leishmania infection among immunocompetent hosts, a community-based study in Chiang Rai, Thailand. PLoS Negl. Trop. Dis. 15, e0009545. https://doi.org/10.1371/journal.pntd.0009545 (2021).
doi: 10.1371/journal.pntd.0009545 pubmed: 34252099 pmcid: 8297947
Ait Kbaich, M. et al. Population structure of Leishmania major in southeastern morocco. Acta Trop. 210, 105587. https://doi.org/10.1016/j.actatropica.2020.105587 (2020).
doi: 10.1016/j.actatropica.2020.105587 pubmed: 32535066
El Hamouchi, A. et al. Epidemiological features of a recent zoonotic cutaneous leishmaniasis outbreak in Zagora province, southern Morocco. PLoS Negl. Trop. Dis. 13, e0007321. https://doi.org/10.1371/journal.pntd.0007321 (2019).
doi: 10.1371/journal.pntd.0007321 pubmed: 30964864 pmcid: 6474635
Tajima, F. The effect of change in population size on DNA polymorphism. Genetics 123, 597–601 (1989).
doi: 10.1093/genetics/123.3.597 pubmed: 2599369 pmcid: 1203832
Fu, Y. X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925 (1997).
doi: 10.1093/genetics/147.2.915 pubmed: 9335623 pmcid: 1208208
Larsson, H., Källman, T., Gyllenstrand, N. & Lascoux, M. Distribution of long-range linkage disequilibrium and Tajima’s D values in Scandinavian populations of Norway spruce (Picea abies). G3 Genes Genom. Genet. 3, 795. https://doi.org/10.1534/g3.112.005462 (2013).
doi: 10.1534/g3.112.005462
Hall, T. A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser. 41, 95–98 (1999).
Stamatakis, A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006).
doi: 10.1093/bioinformatics/btl446 pubmed: 16928733
Silvestro, D. & Michalak, I. raxmlGUI: A graphical front-end for RAxML. Org. Divers. Evol. 12, 335–337 (2012).
doi: 10.1007/s13127-011-0056-0
Rozas, J. et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299–3302. https://doi.org/10.1093/molbev/msx248 (2017).
doi: 10.1093/molbev/msx248 pubmed: 29029172
Leigh, J. W. & Bryant, D. POPART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116. https://doi.org/10.1111/2041-210X.12410 (2015).
doi: 10.1111/2041-210X.12410

Auteurs

Toon Ruang-Areerate (T)

Department of Parasitology, Phramongkutklao College of Medicine, Bangkok, 10400, Thailand. youangtr@yahoo.com.

Panthita Ruang-Areerate (P)

BIOTEC, National Science and Technology Development Agency (NSTDA), Pathum Thani, 12120, Thailand.

Jipada Manomat (J)

Department of Microbiology, Faculty of Science, Mahidol University, Bangkok, 10400, Thailand.

Tawee Naaglor (T)

Department of Parasitology, Phramongkutklao College of Medicine, Bangkok, 10400, Thailand.

Phunlerd Piyaraj (P)

Department of Parasitology, Phramongkutklao College of Medicine, Bangkok, 10400, Thailand.

Mathirut Mungthin (M)

Department of Parasitology, Phramongkutklao College of Medicine, Bangkok, 10400, Thailand.

Saovanee Leelayoova (S)

Department of Parasitology, Phramongkutklao College of Medicine, Bangkok, 10400, Thailand.

Suradej Siripattanapipong (S)

Department of Microbiology, Faculty of Science, Mahidol University, Bangkok, 10400, Thailand. suradej.sir@mahidol.ac.th.

Classifications MeSH