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Molecular typing of Strongyloides stercoralis in Latin America, the clinical connection

Published online by Cambridge University Press:  06 September 2021

Silvia Analía Repetto ,
Juan Quarroz Braghini Open the ORCID record for Juan Quarroz Braghini [Opens in a new window] ,
Marikena Guadalupe Risso ,
Lisana Belén Argüello ,
Estela Inés Batalla ,
Daniel Ricardo Stecher ,
Mariela Fernanda Sierra ,
Juan Miguel Burgos ,
Marcelo Víctor Radisic  and
Stella Maris González Cappa
...Show all authors
Silvia Analía Repetto
Affiliation:
Universidad de Buenos Aires, Facultad de Medicina, Departamento de Microbiología, Buenos Aires, Argentina CONICET - Universidad de Buenos Aires, Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPaM), Buenos Aires, Argentina Universidad de Buenos Aires, Hospital de Clínicas “José de San Martín”, División Infectología, Buenos Aires, Argentina
Juan Quarroz Braghini
Affiliation:
Universidad de Buenos Aires, Facultad de Medicina, Departamento de Microbiología, Buenos Aires, Argentina CONICET - Universidad de Buenos Aires, Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPaM), Buenos Aires, Argentina
Marikena Guadalupe Risso
Affiliation:
Universidad de Buenos Aires, Facultad de Medicina, Departamento de Microbiología, Buenos Aires, Argentina CONICET - Universidad de Buenos Aires, Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPaM), Buenos Aires, Argentina
Lisana Belén Argüello
Affiliation:
Universidad de Buenos Aires, Facultad de Medicina, Departamento de Microbiología, Buenos Aires, Argentina CONICET - Universidad de Buenos Aires, Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPaM), Buenos Aires, Argentina
Estela Inés Batalla
Affiliation:
Universidad de Buenos Aires, Facultad de Medicina, Departamento de Microbiología, Buenos Aires, Argentina CONICET - Universidad de Buenos Aires, Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPaM), Buenos Aires, Argentina
Daniel Ricardo Stecher
Affiliation:
Universidad de Buenos Aires, Hospital de Clínicas “José de San Martín”, División Infectología, Buenos Aires, Argentina
Mariela Fernanda Sierra
Affiliation:
Universidad de Buenos Aires, Hospital de Clínicas “José de San Martín”, División Infectología, Buenos Aires, Argentina
Juan Miguel Burgos
Affiliation:
Instituto de Investigaciones Biotecnológicas, Universidad Nacional de San Martín, Buenos Aires, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Marcelo Víctor Radisic
Affiliation:
División de Enfermedades Infecciosas, Instituto de Nefrología/Nephrology, Buenos Aires, Argentina
Stella Maris González Cappa
Affiliation:
Universidad de Buenos Aires, Facultad de Medicina, Departamento de Microbiología, Buenos Aires, Argentina CONICET - Universidad de Buenos Aires, Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPaM), Buenos Aires, Argentina
Paula Ruybal*
Affiliation:
Universidad de Buenos Aires, Facultad de Medicina, Departamento de Microbiología, Buenos Aires, Argentina CONICET - Universidad de Buenos Aires, Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPaM), Buenos Aires, Argentina
*
Author for correspondence: Paula Ruybal, E-mail: [email protected]
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Abstract

This study analysed Strongyloides stercoralis genetic variability based on a 404 bp region of the cox1 gene from Latin-American samples in a clinical context including epidemiological, diagnosis and follow-up variables. A prospective, descriptive, observational study was conducted to evaluate clinical and parasitological evolution after ivermectin treatment of 41 patients infected with S. stercoralis. Reactivation of the disease was defined both by clinical symptoms appearance and/or direct larvae detection 30 days after treatment or later. We described 10 haplotypes organized in two clusters. Most frequent variants were also described in the Asian continent in human (HP24 and HP93) and canine (HP24) samples. Clinical presentation (intestinal, severe, cutaneous and asymptomatic), immunological status and eosinophil count were not associated with specific haplotypes or clusters. Nevertheless, presence of cluster 1 haplotypes during diagnosis increased the risk of reactivation with an odds ratio (OR) of 7.51 [confidence interval (CI) 95% 1.38–44.29, P = 0.026]. In contrast, reactivation probability was 83 times lower if cluster 2 (I152V mutation) was detected (OR = 0.17, CI 95% 0.02–0.80, P = 0.02). This is the first analysis of S. stercoralis cox1 diversity in the clinical context. Determination of clusters during the diagnosis could facilitate and improve the design of follow-up strategies to prevent severe reactivations of this chronic disease.

Keywords

Cytochrome c oxidase subunit 1follow-upStrongyloides stercoralisstrongyloidiasis reactivation
Type
Research Article
Information
Parasitology , Volume 149 , Issue 1 , January 2022 , pp. 24 - 34
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

References

Al Rawi, S, Louvet-Vallee, S, Djeddi, A, Sachse, M, Culetto, E, Hajjar, C, Boyd, L, Legouis, R and Galy, V (2011) Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science (New York, N.Y.) 334, 1144–1147.10.1126/science.1211878CrossRefGoogle ScholarPubMed
Ashford, RW, Barnish, G and Viney, ME (1992) Strongyloides fuelleborni kellyi: infection and disease in Papua New Guinea. Parasitology Today 8, 314–318.10.1016/0169-4758(92)90106-CCrossRefGoogle ScholarPubMed
Ballard, JWO and Rand, DM (2005) The population biology of mitochondrial DNA and its phylogenetic implications. Annual Review of Ecology, Evolution, and Systematics 36, 621–642.10.1146/annurev.ecolsys.36.091704.175513CrossRefGoogle Scholar
Barratt, JLNN, Lane, M, Talundzic, E, Richins, T, Robertson, G, Formenti, F, Pritt, B, Verocai, G, Nascimento de Souza, J, Mato Soares, N, Traub, R, Buonfrate, D, Bradbury, RS, De Souza, JN, Soares, NM, Traub, R, Buonfrate, D, Bradbury, RS, Nascimento de Souza, J, Mato Soares, N, Traub, R, Buonfrate, D and and Bradbury, RS (2019) A global genotyping survey of Strongyloides stercoralis and Strongyloides fuelleborni using deep amplicon sequencing. PLoS Neglected Tropical Diseases 13, e0007609.10.1371/journal.pntd.0007609CrossRefGoogle ScholarPubMed
Basso, W, Grandt, L-M, Magnenat, A-L, Gottstein, B and Campos, M (2019) Strongyloides stercoralis infection in imported and local dogs in Switzerland: from clinics to molecular genetics. Parasitology Research 118, 255–266.10.1007/s00436-018-6173-3CrossRefGoogle ScholarPubMed
Blouin, MS (1998) Mitochondrial DNA diversity in nematodes. Journal of Helminthology 72, 285–289.10.1017/S0022149X00016618CrossRefGoogle ScholarPubMed
Blouin, MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527–531.10.1016/S0020-7519(01)00357-5CrossRefGoogle ScholarPubMed
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.10.1038/nmeth.2109CrossRefGoogle ScholarPubMed
Dingley, SD, Polyak, E, Ostrovsky, J, Srinivasan, S, Lee, I, Rosenfeld, AB, Tsukikawa, M, Xiao, R, Selak, MA, Coon, JJ, Hebert, AS, Grimsrud, PA, Kwon, YJ, Pagliarini, DJ, Gai, X, Schurr, TG, Hüttemann, M, Nakamaru-Ogiso, E and Falk, MJ (2014) Mitochondrial DNA variant in COX1 subunit significantly alters energy metabolism of geographically divergent wild isolates in Caenorhabditis elegans. Journal of Molecular Biology 426, 2199–2216.10.1016/j.jmb.2014.02.009CrossRefGoogle ScholarPubMed
Fadaei Tehrani, M, Sharifdini, M, Zahabiun, F, Latifi, R and Kia, EB (2019) Molecular characterization of human isolates of Strongyloides stercoralis and Rhabditis spp. based on mitochondrial cytochrome c oxidase subunit 1 (cox1). BMC Infectious Diseases 19, 776.10.1186/s12879-019-4407-3CrossRefGoogle ScholarPubMed
Hasegawa, H, Sato, H, Fujita, S, Nguema, PPM, Nobusue, K, Miyagi, K, Kooriyama, T, Takenoshita, Y, Noda, S, Sato, A, Morimoto, A, Ikeda, Y and Nishida, T (2010) Molecular identification of the causative agent of human strongyloidiasis acquired in Tanzania: dispersal and diversity of Strongyloides spp. and their hosts. Parasitology International 59, 407–413.10.1016/j.parint.2010.05.007CrossRefGoogle ScholarPubMed
Hasegawa, H, Kalousova, B, McLennan, MR, Modry, D, Profousova-Psenkova, I, Shutt-Phillips, KA, Todd, A, Huffman, MA and Petrzelkova, KJ (2016) Strongyloides infections of humans and great apes in Dzanga-Sangha Protected Areas, Central African Republic and in degraded forest fragments in Bulindi, Uganda. Parasitology International 65, 367–370.10.1016/j.parint.2016.05.004CrossRefGoogle ScholarPubMed
Hu, M, Chilton, NB and Gasser, RB (2003) The mitochondrial genome of Strongyloides stercoralis (Nematoda) – idiosyncratic gene order and evolutionary implications. International Journal for Parasitology 33, 1393–1408.10.1016/S0020-7519(03)00130-9CrossRefGoogle ScholarPubMed
Jaleta, TG, Zhou, S, Bemm, FM, Schär, F, Khieu, V, Muth, S, Odermatt, P, Lok, JB and Streit, A (2017) Different but overlapping populations of Strongyloides stercoralis in dogs and humans – dogs as a possible source for zoonotic strongyloidiasis. PLoS Neglected Tropical Diseases 11, e0005752.10.1371/journal.pntd.0005752CrossRefGoogle ScholarPubMed
Kern, EMA, Kim, T and Park, J-K (2020) The mitochondrial genome in nematode phylogenetics. Frontiers in Ecology and Evolution 8, 250.10.3389/fevo.2020.00250CrossRefGoogle Scholar
Kikuchi, T, Hino, A, Tanaka, T, Aung, MPPTHH, Afrin, T, Nagayasu, E, Tanaka, R, Higashiarakawa, M, Win, KK, Hirata, T, Htike, WW, Fujita, J and Maruyama, H (2016) Genome-wide analyses of individual Strongyloides stercoralis (Nematoda: Rhabditoidea) provide insights into population structure and reproductive life cycles. PLoS Neglected Tropical Diseases 10, e0005253.10.1371/journal.pntd.0005253CrossRefGoogle ScholarPubMed
Konrad, A, Thompson, O, Waterston, RH, Moerman, DG, Keightley, PD, Bergthorsson, U and Katju, V (2017) Mitochondrial mutation rate, spectrum and heteroplasmy in Caenorhabditis elegans spontaneous mutation accumulation lines of differing population size. Molecular Biology and Evolution 34, 1319–1334.Google ScholarPubMed
Kumar, S, Stecher, G, Tamura, K and Dudley, J (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets downloaded from. Molecular Biology and Evolution 33, 1870–1874.10.1093/molbev/msw054CrossRefGoogle Scholar
Laymanivong, S, Hangvanthong, B, Insisiengmay, B, Vanisaveth, V, Laxachack, P, Jongthawin, J, Sanpool, O, Thanchomnang, T, Sadaow, L, Phosuk, I, Rodpai, R, Maleewong, W and Intapan, PM (2016) First molecular identification and report of genetic diversity of Strongyloides stercoralis, a current major soil-transmitted helminth in humans from Lao People's Democratic Republic. Parasitology Research 115, 2973–2980.10.1007/s00436-016-5052-zCrossRefGoogle ScholarPubMed
Leigh, JW and Bryant, D (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.10.1111/2041-210X.12410CrossRefGoogle Scholar
Nagayasu, E, Aung, MPPTHH, Hortiwakul, T, Hino, A, Tanaka, T, Higashiarakawa, M, Olia, A, Taniguchi, T, Win, SMT, Ohashi, I, Odongo-Aginya, EI, Aye, KM, Mon, M, Win, KK, Ota, K, Torisu, Y, Panthuwong, S, Kimura, E, Palacpac, NMQ, Kikuchi, T, Hirata, T, Torisu, S, Hisaeda, H, Horii, T, Fujita, J, Htike, WW and Maruyama, H (2017) A possible origin population of pathogenic intestinal nematodes, Strongyloides stercoralis, unveiled by molecular phylogeny. Scientific Reports 7, 4844.10.1038/s41598-017-05049-xCrossRefGoogle ScholarPubMed
Repetto, SA, Durán, PA, Lasala, MB and González-Cappa, SM (2010) High rate of strongyloidosis infection, out of endemic area, in patients with eosinophilia and without risk of exogenous reinfections. The American Journal of Tropical Medicine and Hygiene 82, 1088–1093.10.4269/ajtmh.2010.09-0332CrossRefGoogle ScholarPubMed
Repetto, SA, Soto, CDA, Cazorla, SI, Tayeldin, ML, Cuello, S, Lasala, MB, Tekiel, VS and González Cappa, SM (2013) An improved DNA isolation technique for PCR detection of Strongyloides stercoralis in stool samples. Acta Tropica 126, 110–114.10.1016/j.actatropica.2013.02.003CrossRefGoogle ScholarPubMed
Repetto, SA, Ruybal, P, Solana, ME, López, C, Berini, CA, Alba Soto, CD and Cappa, SMG (2016) Comparison between PCR and larvae visualization methods for diagnosis of Strongyloides stercoralis out of endemic area: a proposed algorithm. Acta Tropica 157, 169–177.10.1016/j.actatropica.2016.02.004CrossRefGoogle ScholarPubMed
Repetto, SA, Ruybal, P, Batalla, E, López, C, Fridman, V, Sierra, M, Radisic, M, Bravo, PM, Risso, MG, González Cappa, SM and Alba Soto, CD (2018 a) Reply to Buonfrate and Bisoffi. Clinical Infectious Diseases 67, 811–812.10.1093/cid/ciy178CrossRefGoogle ScholarPubMed
Repetto, SA, Ruybal, P, Batalla, E, López, C, Fridman, V, Sierra, M, Radisic, M, Bravo, PM, Risso, MG, González Cappa, SM and Alba Soto, CD (2018 b) Strongyloidiasis outside endemic areas: long-term parasitological and clinical follow-up after ivermectin treatment. Clinical Infectious Diseases 66, 1558–156510.1093/cid/cix1069CrossRefGoogle ScholarPubMed
Rozas, J, Ferrer-Mata, A, Carlos anchez-DelBarrio, JS, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Anchez-Gracia, AS (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 3299–3302.10.1093/molbev/msx248CrossRefGoogle ScholarPubMed
Sanpool, O, Intapan, PM, Rodpai, R, Laoraksawong, P, Sadaow, L, Tourtip, S, Piratae, S, Maleewong, W and Thanchomnang, T (2020) Dogs are reservoir hosts for possible transmission of human strongyloidiasis in Thailand: molecular identification and genetic diversity of causative parasite species. Journal of Helminthology 94, e110.10.1017/S0022149X1900107XCrossRefGoogle Scholar
Sato, M and Sato, K (2013) Maternal inheritance of mitochondrial DNA by diverse mechanisms to eliminate paternal mitochondrial DNA. Biochimica et Biophysica Acta (BBA) – Molecular Cell Research 1833, 1979–1984.10.1016/j.bbamcr.2013.03.010CrossRefGoogle ScholarPubMed
Savioli, L, Bundy, DAP and Mundial, B (2014) WGO practice guidelines: Manejo de la Estrongiloidiasis Manejo de la Estrongiloidiasis. WGO Practice Guidelines, 5–7.Google Scholar
Schär, F, Trostdorf, U, Giardina, F, Khieu, V, Muth, S, Marti, H, Vounatsou, P and Odermatt, P (2013) Strongyloides stercoralis: global distribution and risk factors. PLoS Neglected Tropical Diseases 7, e2288.10.1371/journal.pntd.0002288CrossRefGoogle ScholarPubMed
Spotin, A, Mahami-Oskouei, M and Nami, S (2019) Assessment of the global paradigms of genetic variability in Strongyloides stercoralis infrapopulations determined by mitochondrial DNA sequences. Comparative Immunology. Microbiology and Infectious Diseases 67, 101354. doi: 10.1016/j.cimid.2019.101354CrossRefGoogle ScholarPubMed
Stephens, M and Donnelly, P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics 73, 1162–1169.10.1086/379378CrossRefGoogle ScholarPubMed
Thanchomnang, T, Intapan, PM, Sanpool, O, Rodpai, R, Tourtip, S, Yahom, S, Kullawat, J, Radomyos, P, Thammasiri, C and Maleewong, W (2017) First molecular identification and genetic diversity of Strongyloides stercoralis and Strongyloides fuelleborni in human communities having contact with long-tailed macaques in Thailand. Parasitology Research 116, 1917–1923.10.1007/s00436-017-5469-zCrossRefGoogle ScholarPubMed
Tomasini, N, Lauthier, JJ, Llewellyn, MS and Diosque, P (2013) MLSTest: Novel software for multi-locus sequence data analysis in eukaryotic organisms. Infection Genetics and Evolution 20, 188–196.10.1016/j.meegid.2013.08.029CrossRefGoogle ScholarPubMed
Wernick, RI, Estes, S, Howe, DK and Denver, DR (2016) Paths of heritable mitochondrial DNA mutation and heteroplasmy in reference and gas-1 strains of Caenorhabditis elegans. Frontiers in Genetics 7, 51.10.3389/fgene.2016.00051CrossRefGoogle ScholarPubMed
Zhou, Q, Li, H and Xue, D (2011) Elimination of paternal mitochondria through the lysosomal degradation pathway in C. elegans. Cell Research 21, 1662–1669.CrossRefGoogle ScholarPubMed
Zhou, S, Fu, X, Pei, P, Kucka, M, Liu, J, Tang, L, Zhan, T, He, S, Chan, YF, Rödelsperger, C, Liu, D and Streit, A (2019) Characterization of a non-sexual population of Strongyloides stercoralis with hybrid 18S rDNA haplotypes in Guangxi, Southern China. PLOS Neglected Tropical Diseases 13, e0007396.10.1371/journal.pntd.0007396CrossRefGoogle ScholarPubMed
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