{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,17]],"date-time":"2026-02-17T03:47:12Z","timestamp":1771300032096,"version":"3.50.1"},"reference-count":41,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,6,2]],"date-time":"2021-06-02T00:00:00Z","timestamp":1622592000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,6,2]],"date-time":"2021-06-02T00:00:00Z","timestamp":1622592000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"crossref","award":["DFG Ke428\/13-1"],"award-info":[{"award-number":["DFG Ke428\/13-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Parasites Vectors"],"published-print":{"date-parts":[[2021,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>African trypanosomiases are vector-borne diseases that affect humans and livestock in sub-Saharan Africa. Although data have been collected on tsetse fauna as well as trypanosome infections in tsetse flies and mammals in foci of sleeping sickness in Chad, the situation of tsetse fly-transmitted trypanosomes remains unknown in several tsetse-infested areas of Chad. This study was designed to fill this epidemiological knowledge gap by determining the tsetse fauna as well as the trypanosomes infecting tsetse flies in the area of Lake Iro in southeastern Chad.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>Tsetse flies were trapped along the Salamat River using biconical traps. The proboscis and tsetse body were removed from each fly. DNA was extracted from the proboscis using proteinase K and phosphate buffer and from the tsetse body using Chelex 5%. Tsetse flies were identified by amplifying and sequencing the cytochrome<jats:italic> c<\/jats:italic> oxydase I gene of each tsetse fly. Trypanosome species were detected by amplifying and sequencing the internal transcribed spacer 1 of infecting trypanosomes.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>A total of 617 tsetse flies were trapped; the apparent density of flies per trap per day was 2. 6. Of the trapped flies, 359 were randomly selected for the molecular identification and for the detection of infecting trypanosomes. <jats:italic>Glossina morsitans submorsitans<\/jats:italic> (96.1%) was the dominant tsetse fly species followed by <jats:italic>G. fuscipes fuscipes<\/jats:italic> (3.1%) and <jats:italic>G. tachinoides<\/jats:italic> (0.8%). Four trypanosome species, including <jats:italic>Trypanosoma vivax<\/jats:italic>,<jats:italic> T. simiae<\/jats:italic>, <jats:italic>T. godfreyi<\/jats:italic> and <jats:italic>T. congolense<\/jats:italic> savannah, were detected. Both single infection (56.7%) and mixed infections of trypanosomes (4.6%) were detected in <jats:italic>G. m. submorsitans<\/jats:italic>. The single infection included <jats:italic>T. simiae<\/jats:italic> (20.5%), <jats:italic>T. congolense<\/jats:italic> savannah (16.43%), <jats:italic>T. vivax<\/jats:italic> (11.7%) and <jats:italic>T. godfreyi<\/jats:italic> (9.8%). The trypanosome infection rate was 61.4% in <jats:italic>G. m. submorsitans<\/jats:italic>, 72.7% in <jats:italic>G. f. fuscipes<\/jats:italic> and 66.6% in <jats:italic>G. tachinoides<\/jats:italic>. Trypanosome infections were more prevalent in tsetse bodies (40.6%) than in the proboscis (16.3%).<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusion<\/jats:title>\n                <jats:p>This study revealed the presence of different tsetse species and a diversity of trypanosomes pathogenic to livestock in the area of Lake Iro. The results highlight the risks and constraints that animal African trypanosomiasis pose to livestock breeding and the importance of assessing trypanosome infections in livestock in this area.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Graphical Abstract<\/jats:title>\n                \n              <\/jats:sec>","DOI":"10.1186\/s13071-021-04782-7","type":"journal-article","created":{"date-parts":[[2021,6,2]],"date-time":"2021-06-02T12:11:34Z","timestamp":1622635894000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Diversity of tsetse flies and trypanosome species circulating in the area of Lake Iro in southeastern Chad"],"prefix":"10.1186","volume":"14","author":[{"given":"Djoukzoumka","family":"Signaboubo","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Vincent Khan","family":"Payne","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ibrahim Mahamat Alhadj","family":"Moussa","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hassane Mahamat","family":"Hassane","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Petra","family":"Berger","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Soerge","family":"Kelm","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0449-818X","authenticated-orcid":false,"given":"Gustave","family":"Simo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2021,6,2]]},"reference":[{"key":"4782_CR1","doi-asserted-by":"publisher","first-page":"2397","DOI":"10.1016\/S0140-6736(17)31510-6","volume":"390","author":"P B\u00fcscher","year":"2017","unstructured":"B\u00fcscher P, Cecchi G, Jamonneau V, Priotto G. Human African trypanosomiasis. Lancet. 2017;390:2397\u2013409.","journal-title":"Lancet"},{"key":"4782_CR2","doi-asserted-by":"publisher","first-page":"1496","DOI":"10.1038\/ismej.2014.236","volume":"9","author":"A Geiger","year":"2015","unstructured":"Geiger A, Ponton F, Simo G. Adult blood-feeding tsetse flies, trypanosomes, microbiota and fluctuating environment in sub-Saharan Africa. ISME J. 2015;9:1496\u2013507.","journal-title":"ISME J"},{"issue":"8","key":"4782_CR3","first-page":"12","volume":"4","author":"G Cecchi","year":"2008","unstructured":"Cecchi G, Mattioli RC, Slingenbergh J, De la Rocque S. Land and tsetse distribution in sub-Saharian Africa. Med Vet Entomol. 2008;4(8):12\u201343.","journal-title":"Med Vet Entomol"},{"key":"4782_CR4","first-page":"2277","volume":"3","author":"TTE Angara","year":"2014","unstructured":"Angara TTE, Ismail AA, Ibrahim AM. An overview of the economic impact of animal trypanosomiasis. GJRA. 2014;3:2277\u20138160.","journal-title":"GJRA"},{"key":"4782_CR5","first-page":"369","volume-title":"The trypanosomiases","author":"PM Shaw","year":"2014","unstructured":"Shaw PM. Economics of African trypanosomiasis. In: Maudlin I, Holmes PH, Mile MA, editors. The trypanosomiases. CABI Publishing: Wallingford; 2014. p. 369\u2013402."},{"issue":"1","key":"4782_CR6","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1186\/1756-3305-1-24","volume":"1","author":"SJ Schofiel","year":"2008","unstructured":"Schofiel SJ, Kaboyo JP. Trypanosomiasis vector control in Africa and Latin America. Parasites Vectors. 2008;1(1):24.","journal-title":"Parasites Vectors"},{"issue":"7","key":"4782_CR7","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1016\/j.pt.2017.02.005","volume":"33","author":"O Diall","year":"2017","unstructured":"Diall O, Cecchi G, Wanda G, Argil\u00e9s-Herrero R, Vreysen MJB, Cattoli G, et al. Developing a progressive control pathway for African animal Trypanosomosis. Trends Parasitol. 2017;33(7):499\u2013509.","journal-title":"Trends Parasitol"},{"key":"4782_CR8","doi-asserted-by":"crossref","unstructured":"Mamoudou A, Njanloga A, HayatouA, Suh PF, Achukwui MD. Animal trypanosomiasis in clinical implications healphy cattle of North Cameroon: Epidemiological implication. Parasites Vectors. 2016; 9:206.","DOI":"10.1186\/s13071-016-1498-1"},{"key":"4782_CR9","doi-asserted-by":"publisher","first-page":"631","DOI":"10.1186\/s13071-017-2540-7","volume":"10","author":"SCH Ngomtcho","year":"2017","unstructured":"Ngomtcho SCH, Weber JS, Ngo Bum E, Gbem TT, Kelm S, Achukwi AD. Molecular screening of tsetse flies reveals different trpanosoma species including T grayi and T. theileri in Northern Cameroon. Parasites Vectors. 2017;10:631.","journal-title":"Parasites Vectors"},{"key":"4782_CR10","doi-asserted-by":"publisher","first-page":"805","DOI":"10.1007\/s00436-020-06606-6","volume":"119","author":"NC Kamdem","year":"2020","unstructured":"Kamdem NC, Zebaze TAA, Estelle Mezajou ME, Amih Ofon E, Djoumessi GEB, Simo G. Identification of different trypanosome species in tsetse flies caught in the wildlife reserve of Santchou in the western region of Cameroon. Parasitol Res. 2020;119:805.","journal-title":"Parasitol Res"},{"key":"4782_CR11","unstructured":"Minist\u00e8re de l\u2019\u00e9levage et des productions animales et l\u2019Organisation des Nations Unies pour l\u2019Alimentation et l\u2019Agriculture. Recensement g\u00e9n\u00e9rale de l\u2019\u00e9levage au Tchad. Effectifs du cheptel tchadien: principaux r\u00e9sultats d\u00e9finitifs. 2018. http:\/\/www.fao.org\/tchad\/actualites\/detail-events\/ru\/c\/1128777\/ Accessed 27 Apr 2021."},{"key":"4782_CR12","unstructured":"Hassane Mahamat H. Enqu\u00eate \u00e9pid\u00e9miologique et entomologique de la trypanosomiase et son vecteur dans le bassin du Mandoul. N\u2019Djamena: Laboratoire de Recherche V\u00e9t\u00e9rinaire et Zootechnique. 2003."},{"issue":"1","key":"4782_CR13","doi-asserted-by":"publisher","first-page":"5","DOI":"10.19182\/remvt.10154","volume":"67","author":"P Mallaye","year":"2014","unstructured":"Mallaye P, Tongue LK, Ndeledje N, Hassane MH. Transmission concomitante des trypanosomes humaine et animale: le foyer de Mandoul au Tchad. Rev Elev Med Vet Pays Trop. 2014;67(1):5\u201312.","journal-title":"Rev Elev Med Vet Pays Trop"},{"key":"4782_CR14","unstructured":"Paigbc. Plan d\u2019am\u00e9nagement int\u00e9gr\u00e9 \u00e0 base communautaire, site de Boum Kebir. Minist\u00e8re\u00a0de l\u2019Environnement et des Ressources Halieutiques, Direction des P\u00eaches et\u00a0de\u00a0l\u2019Aquaculture: IRD Edition. 2012."},{"key":"4782_CR15","unstructured":"Boyer JD, Rouche CN, Cres A, Servat E, Paturel J, Mah\u00e9 G. SIEREM: an environnmental information system for water resources. In: 5th World FRIEND Conference. La Havana. 2006. p. 19\u201325."},{"key":"4782_CR16","doi-asserted-by":"crossref","unstructured":"Raimond C, Florence Sylvestre, Zakinet D et Abderamane M. Tchad des lacs: les zones humides sah\u00e9liennes au d\u00e9fi du changement global. IRD \u00c9ditions. 2019. https:\/\/doi.org\/10.4000.books.irdeditions.30450.","DOI":"10.4000\/books.irdeditions.30450"},{"key":"4782_CR17","first-page":"283","volume":"3","author":"C Laveissiere","year":"1973","unstructured":"Laveissiere C. Am\u00e9lioration du rendement du pi\u00e8ge biconique pour glossines (Diptera, Glossinidae) par l\u2019emploi d\u2019un c\u00f4ne inf\u00e9rieur bleu. Entomol Med Parasitol. 1973;3:283\u20136.","journal-title":"Entomol Med Parasitol"},{"key":"4782_CR18","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1016\/j.ympev.2008.07.011","volume":"49","author":"NA Dyer","year":"2008","unstructured":"Dyer NA, Lawton SP, Ravel S, Choi KS, Lehane MJ, Robinson AS, et al. Molecular phylogenetics of tsetse flies (Diptera: Glossinidae) based on mitochondrial (COI, 16S, ND2) and nuclear ribosomal DNA sequences, with an emphasis on the palpalis group. Mol Phylogenet Evol. 2008;49:227\u201339.","journal-title":"Mol Phylogenet Evol"},{"key":"4782_CR19","doi-asserted-by":"publisher","first-page":"167","DOI":"10.2217\/17460913.3.2.167","volume":"3","author":"ER Adams","year":"2008","unstructured":"Adams ER, Hamilton PB. New molecular tools for the identification of trypanosome species. Future Microbiol. 2008;3:167\u201376.","journal-title":"Future Microbiol"},{"key":"4782_CR20","unstructured":"R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. 2010. http:\/\/www.R-project.org\/."},{"issue":"63","key":"4782_CR21","first-page":"12","volume":"27","author":"J Vourchakb\u00e9","year":"2020","unstructured":"Vourchakb\u00e9 J, Tiofact AAZ, Kante ST, Mpoame M, Simo G. Molecular identification of Trypanosoma brucei gambiense in natural infected pigs, dogs and small ruminants confirms domestic animals as potential reservoirs for sleeping sickness in Chad. Parasite. 2020;27(63):12.","journal-title":"Parasite"},{"issue":"13","key":"4782_CR22","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1186\/s13071-020-04192-1","volume":"2020","author":"J Vourchakb\u00e9","year":"2020","unstructured":"Vourchakb\u00e9 J, Tiofact AAZ, Mpoame Mbida G, Simo. Trypanosome infections in naturally infected horses and donkey of three active sleeping sickness foci in Chad. Parasites Vectors. 2020;2020(13):323.","journal-title":"Parasites Vectors"},{"key":"4782_CR23","doi-asserted-by":"publisher","first-page":"169","DOI":"10.19182\/remvt.7408","volume":"19","author":"J Gruvel","year":"1966","unstructured":"Gruvel J. Tse-tse flies as vectors of trypanosomiasis in Chad. Rev Elev Med Vet Pays Trop. 1966;19:169\u2013212.","journal-title":"Rev Elev Med Vet Pays Trop"},{"key":"4782_CR24","unstructured":"Cuisance D. R\u00e9actualisation de la situation des ts\u00e9-ts\u00e9 et des trypanosomoses animales au Tchad. Phase II\/Zone du Lac, Guera, Salamat. Enqu\u00eate r\u00e9alis\u00e9e du 22 mars au 20 avril 1996. CIRAD-EMVT; 1996. https:\/\/agritrop.cirad.fr\/327260\/. Accessed 4 Mar 2021."},{"key":"4782_CR25","doi-asserted-by":"crossref","unstructured":"Shaida SS, Weber SJ, Gbem T, Ngomtcho SCH, Musa UB, Achukwi MD, et al. Diversity and phylogenetic relationships of Glossina populations in Nigeria and the Cameroonian border region. BMC Microbiol. 2018. 18(1):1804.","DOI":"10.1186\/s12866-018-1293-6"},{"key":"4782_CR26","doi-asserted-by":"publisher","first-page":"520","DOI":"10.1186\/s13071-016-1805-x","volume":"9","author":"S Pagabeleguem","year":"2016","unstructured":"Pagabeleguem S, Ravel S, Dicko AH, Vreysen MJB, Parker A, Takac P, et al. Influence of temperature and relative humidity on survival and fecundity of three tsetse strains. Parasites Vectors. 2016;9:520.","journal-title":"Parasites Vectors"},{"key":"4782_CR27","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1016\/S0167-8809(99)00103-6","volume":"77","author":"R Reid","year":"2000","unstructured":"Reid R, Kruska RL, Deitchmann U, Thotthon PK, Leak SGA. Human population growth and the extinction of the tsetse fly. Agric Ecosyst Environ. 2000;77:227\u201336.","journal-title":"Agric Ecosyst Environ"},{"key":"4782_CR28","unstructured":"Dejace P, Laure Gautsr ER, Philippe Bouch\u00e9. Les populations de grands mammif\u00e8res et d\u2019autruches du Parc National de Zakouma au Tchad statut et tendance d\u2019evolution. Rev Ecol. 2000;5(55):111\u201334."},{"key":"4782_CR29","unstructured":"Potgieter D, Dogringar, S, Djimet, B, Lamoureaux, S. Dry season aerial total count. Zakouma National Park. Chad. Unpublished report. New York: Wildlife Conservation Society; 2011."},{"key":"4782_CR30","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1186\/s13071-019-3718-y","volume":"12","author":"JS Weber","year":"2019","unstructured":"Weber JS, Ngomtcho SCH, Shaida SS, Chechet GD, Gbem TT, Nok JA, et al. Genetic diversity of trypanosome species in tsetse flies (Glossina spp.) in Nigeria. Parasites Vectors. 2019;12:481.","journal-title":"Parasites Vectors"},{"key":"4782_CR31","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1186\/s13071-016-1585-3","volume":"9","author":"C Isaac","year":"2016","unstructured":"Isaac C, Ciosi M, Hamilton A, Scullion KM, Dede P, Igbinosa IB, et al. Molecular identification of different trypanosome species and subspecies in tsetse flies of northern Nigeria. Parasites Vectors. 2016;9:301.","journal-title":"Parasites Vectors"},{"key":"4782_CR32","doi-asserted-by":"publisher","first-page":"115","DOI":"10.3389\/fcimb.2016.00115","volume":"6","author":"C-P Ooi","year":"2016","unstructured":"Ooi C-P, Schuster S, Cren-Travaill\u00e9 C, Bertiaux E, Cosson A, Goyard S, et al. The cyclical development of Trypanosoma vivax in the tsetse fly involves an asymmetric division. Front Cell Infect Microbiol. 2016;6:115. https:\/\/doi.org\/10.3389\/fcimb.2016.00115.","journal-title":"Front Cell Infect Microbiol"},{"key":"4782_CR33","first-page":"50","volume":"29","author":"L Penchenier","year":"1996","unstructured":"Penchenier L, Bodo JM, Bureau PH, Morlais I, Djoha S, Herder S. Utilisation de la PCR sur sang pour le diagnostic des trypanosomiases porcines. Bull Liaison Doc OCEAC. 1996;29:50\u20133.","journal-title":"Bull Liaison Doc OCEAC"},{"key":"4782_CR34","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/j.vetpar.2006.02.026","volume":"139","author":"G Simo","year":"2006","unstructured":"Simo G, Aonganyi T, Nkinin SW, Njiokou F, Herder S. High prevalence of Trypanosoma brucei gambiense groupe 1 in the pigs from Fontem sleeping sickness focus in Cameroon. Vet Parasitol. 2006;139:57\u201366.","journal-title":"Vet Parasitol"},{"key":"4782_CR35","unstructured":"Swallow BM. Impact of trypanosomiasis on African agriculture. PAAT Technical and Scientific Series. Rome: FAO; 2000.http:\/\/www.fao.org\/3\/X4755EN\/x4755en.pdf. Accessed 27 Apr 2021."},{"key":"4782_CR36","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/0001-706X(90)90063-6","volume":"48","author":"JMC Trail","year":"2000","unstructured":"Trail JMC, D\u2019Ietem GDM, Feron A, Kankiese O, Mulungo M, Pelo M. Effect of trypanosomes infection, control of parasitaemia and control of anaemia development on productivity of N\u2019dama cattle. Acta Trop. 2000;48:37\u201345.","journal-title":"Acta Trop"},{"issue":"3\u20134","key":"4782_CR37","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1016\/0001-706X(92)90045-Y","volume":"51","author":"SK Moloo","year":"1992","unstructured":"Moloo SK, Sabwa CL, Kabata JM. Vector competence of Glossina pallidipes and G. morsitans cetralis  for Trypanosoma vivax, T. congolense, and T. b. brucei. Acta Trop. 1992;51(3\u20134):271\u201380.","journal-title":"Acta Trop."},{"issue":"5","key":"4782_CR38","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1080\/00034983.1992.11812703","volume":"86","author":"SC Welburn","year":"1992","unstructured":"Welburn SC, Maudlin I. The nature of the teneral state in Glossina and its role in the acquisition of trypanosome infection in tsetse. Ann Trop Med Parasitol. 1992;86(5):529\u201336.","journal-title":"Ann Trop Med Parasitol"},{"issue":"7","key":"4782_CR39","first-page":"186","volume":"5","author":"M Desta","year":"2013","unstructured":"Desta M, Menkir S, Kebede A. The study on tsetse fly (Glossina species) and their role in trypanosome infection rate in Birbir valley, Baro Akobo River system, western Ethiopia. J Vet Med Anim Health. 2013;5(7):186\u201394.","journal-title":"J Vet Med Anim Health"},{"key":"4782_CR40","doi-asserted-by":"publisher","first-page":"693","DOI":"10.1017\/S0031182004005876","volume":"129","author":"V Jamonneau","year":"2004","unstructured":"Jamonneau V, Ravel S, Koffi M, Kaba D, Zeze DG, Ndri L, et al. Mixed infections of trypanosomes in tsetse and pigs and their epidemiological significance in a sleeping sickness focus of C\u00f4te d\u2019Ivoire. Parasitology. 2004;129:693\u2013702.","journal-title":"Parasitology"},{"issue":"6","key":"4782_CR41","doi-asserted-by":"publisher","first-page":"1035","DOI":"10.1093\/jmedent\/42.6.1035","volume":"42","author":"C Kubi","year":"2005","unstructured":"Kubi C, Van Abbelle J, Dorny P, Coosemans M, Marcotty T, Andp T, et al. Ability of trypanosome-infected tsetse flies (Diptera: Glossinidae) to acquire an infection with a second trypanosome species. J Med Entomol. 2005;42(6):1035\u20138.","journal-title":"J Med Entomol"}],"container-title":["Parasites &amp; Vectors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13071-021-04782-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13071-021-04782-7\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13071-021-04782-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,11,15]],"date-time":"2021-11-15T17:05:11Z","timestamp":1636995911000},"score":1,"resource":{"primary":{"URL":"https:\/\/parasitesandvectors.biomedcentral.com\/articles\/10.1186\/s13071-021-04782-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,2]]},"references-count":41,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12]]}},"alternative-id":["4782"],"URL":"https:\/\/doi.org\/10.1186\/s13071-021-04782-7","relation":{},"ISSN":["1756-3305"],"issn-type":[{"value":"1756-3305","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,2]]},"assertion":[{"value":"24 February 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 May 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 June 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"293"}}