Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-04T19:18:45.519Z Has data issue: false hasContentIssue false
  • English
  • Français

Hepatozoon milleri sp. nov. (Adeleorina: Hepatozoidae) in Akodon montensis (Rodentia: Cricetidae: Sigmodontinae) from southeastern Brazil

Published online by Cambridge University Press:  29 November 2018

Larissa de Castro Demoner ,
Maria Regina Lucas da Silva ,
Natalia Mizuhira Magro  and
Lucia Helena O'Dwyer Open the ORCID record for Lucia Helena O'Dwyer [Opens in a new window]
Larissa de Castro Demoner
Affiliation:
Hospital Veterinário-Universidade Federal Rural do Semi-árido, Mossoró, Brazil
Maria Regina Lucas da Silva
Affiliation:
Universidade Estadual Paulista (UNESP), Instituto de Biociências, Departamento de Parasitologia, Campus de Botucatu, Distrito de Rubião Junior, Botucatu, São Paulo, Brazil
Natalia Mizuhira Magro
Affiliation:
Universidade Estadual Paulista (UNESP), Instituto de Biociências, Departamento de Parasitologia, Campus de Botucatu, Distrito de Rubião Junior, Botucatu, São Paulo, Brazil
Lucia Helena O'Dwyer*
Affiliation:
Universidade Estadual Paulista (UNESP), Instituto de Biociências, Departamento de Parasitologia, Campus de Botucatu, Distrito de Rubião Junior, Botucatu, São Paulo, Brazil
*
Author for correspondence: Lucia Helena O'Dwyer, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Members of the genus Hepatozoon (Miller, 1908) are blood parasites found in a wide range of host species, including wild rodents; however, information about the life cycle, distribution and Hepatozoon species diversity infecting these mammals are lacking. We studied the parasite stages and DNA sequences of Hepatozoon sp. of 11 naturally infected Akodon montensis. Thin blood smears, tissue samples and whole blood were obtained for morphology, morphometry and molecular analyses. Seven of the 11 rodents had gamonts on the blood smears. Biological and morphological features of the parasite such as tissue tropism, gamonts and meronts size and morphology, as well as the DNA sequence comparison and phylogenetic analysis, indicated that the Hepatozoon sp. detected in this study is distinct from those species previously reported in small rodents. Herein, we propose a new species, named Hepatozoon milleri sp. nov. This is the first description of a new Hepatozoon species from wild small rodents in Brazil, based on morphological and molecular characteristics.

Keywords

BrazilHepatozoonmolecular characterizationnew speciesparasite stagesrodent
Type
Research Article
Information
Parasitology , Volume 146 , Issue 5 , April 2019 , pp. 662 - 669
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

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

Aktas, M, Özübek, S, Altay, K, Balkaya, I, Utuk, AE, Kırbase, A, Simsek, S and Dumanlı, N (2015) A molecular and parasitological survey of Hepatozoon canis in domestic dogs in Turkey. Veterinary Parasitology 209, 264–267.Google Scholar
Allen, KE, Yabsley, MJ, Johnson, EM, Reichard, MV, Panciera, RJ, Ewing, SA and Little, SE (2011) Novel Hepatozoon in vertebrates from the southern United States. Journal of Parasitology 94, 648–653.Google Scholar
André, MR, Adania, CH, Teixeira, RHF, Vargas, GH, Falcade, M, Sousa, L, Salles, AR, Allegretti, SM, Felippe, PAN and Machado, RZ (2010) Molecular detection of Hepatozoon spp. in Brazilian and exotic wild carnivores. Veterinary Parasitology 173, 134–138.Google Scholar
Balfour, A (1905) A haemogregarine of mammals. The Journal of Tropical Medicine 8, 241.Google Scholar
Baneth, G, Samish, M and Shkap, V (2007) Life cycle of Hepatozoon canis (Apicomplexa: Adeleorina: Hepatozoidae) in the tick Rhipicephalus sanguineus and domestic dog (Canis familiaris). Journal of Parasitology 93, 283–299.Google Scholar
Barta, JR, Ogedengbe, JD, Martin, DS and Smith, TG (2012) Phylogenetic position of the adeleorinid Coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) inferred using 18S rDNA sequences. Journal of Eukaryotic Microbiology 59, 171–180.Google Scholar
Borges-Nojosa, DM, Borges-Leite, MJ, Maia, JP, Zanchi-Silva, D, da Rocha Braga, R and Harris, DJ (2017) A new species of Hepatozoon miller, 1908 (Apicomplexa: Adelerina) from the snake Philodryas nattereri Steindachner (Squamata: Dipsadidae) in northeastern Brazil. Systematic Parasitology 94, 65–72.Google Scholar
Breshears, MA, Kocan, KM, Johnson, EM and Panciera, RJ (2009) Light and transmission electron microscopic characteristics of a novel Hepatozoon spp. in naturally infected cotton rats (Sigmodon hispidus). Parasitology Research 105, 1327–1332.Google Scholar
Carini, A (1910) Sobre a ‘haemogregarina muris’. Revista Medica de São Paulo 5, 347–349.Google Scholar
Carini, A and Maciel, J (1915) Sur une hémogrégarine et un trypanosome d'un Muridé (Akodon fuliginosus). Bulletin de la Société de Pathológie Exotique 8, 165–169.Google Scholar
Cook, CA, Netherlands, EC and Smit, NJ (2015) First Hemolivia from Southern Africa: reassigning chelonian Haemogregarina parvula Dias, 1953 (Adeleorina: Haemogregarinidae) to Hemolivia (adeleorina: Karyolysidae). African Zoology 50, 165–173.Google Scholar
Criado-Fornelio, A, Ruas, JL, Casado, N, Farias, NAR, Soares, MP, Müller, G, Brum, JGW, Berne, MEA, Buling-Saraña, A and Barba-Carretero, JC (2006) New molecular data on mammalian Hepatozoon species (Apicomplexa: Adeleorina) from Brazil and Spain. Journal of Parasitology 92, 93–99.Google Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.Google Scholar
Davidson, WR and Calpin, JP (1976) Hepatozoon griseisciuri infection in gray squirrels of the southeastern United States. Journal of Wildlife Diseases 12, 72–76.Google Scholar
Demoner, LC, Magro, NM, da Silva, MRL, Antunes, JMAP, Calabuig, CIP and O'Dwyer, LH (2016) Hepatozoon spp. infections in wild rodents in an area of endemic canine hepatozoonosis in southeastern Brazil. Ticks and Tick-borne Diseases 7, 859–864.Google Scholar
Desser, SS (1990) Tissue ‘cysts’ of Hepatozoon griseisciuri in the grey squirrel, Sciurus carolinensis: the significance of these cysts in species of Hepatozoon. Journal of Parasitology 76, 257–259.Google Scholar
Duscher, GG, Leschnik, M, Fuehrer, HP and Joachim, A (2014) Wildlife reservoirs for vector-borne canine, feline and zoonotic infections in Austria. International Journal for Parasitology: Parasites and Wildlife 4, 88–96.Google Scholar
Ewing, SA and Panciera, RJ (2003) American canine Hepatozoonosis. Clinical Microbiology Review 16, 688–697.Google Scholar
Farkas, R, Solymosi, N, Takács, N, Ákos, H, Hornok, S, Nachum-Biala, Y and Baneth, G (2014) First molecular evidence of Hepatozoon canis infection in red foxes and golden jackals from Hungary. Parasites and Vectors 7, 1–7.Google Scholar
Harikrishnan, TJ, Ponnudurai, G and Anna, T (2011) Some observations on Hepatozoon muris in brown rats (Rattus norvegicus). Journal of Veterinary Parasitology 25, 72–75.Google Scholar
Homan, WL, Vercammen, M, De Braekeleer, J and Verschueren, H (2000) Identification of a 200- to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. International Journal of Parasitology 30, 69–75.Google Scholar
Johnson, EM, Allen, KE, Panciera, RJ, Ewing, SA, Little, SE and Reichard, MV (2007) Field survey of rodents for Hepatozoon infections in an endemic focus of American canine hepatozoonosis. Veterinary Parasitology 150, 27–32.Google Scholar
Johnson, EM, Allen, KE, Panciera, RJ, Little, SE and Ewing, SA (2008) Infectivity of Hepatozoon americanum cystozoites for a dog. Veterinary Parasitology 154, 148–150.Google Scholar
Kamani, J, Harrus, S, Nachum-Biala, Y, Gutiérrez, R, Mumcuoglu, KY and Baneth, G (2018) Prevalence of Hepatozoon and Sarcocystis spp. in rodents and their ectoparasites in Nigeria. Acta Tropica 187, 124–128.Google Scholar
Kiernan, JA (2015) Histological and Histochemical Methods. Theory & Practice, 5th edn. Banbury, UK: Scion Publishing, 571 pp.Google Scholar
Laakkonen, J, Sukura, A, Oksanen, A, Henttonen, H and Soveri, T (2001) Haemogregarines of the genus Hepatozoon (apicomplexa: Adeleina) in rodents from Northern Europe. Folia Parasitologica 48, 263–267.Google Scholar
Laird, M (1951) Blood parasites of Mammals in New Zealand. Zoology Publications 9, 5–8.Google Scholar
Laison, R, Paperna, I and Naiff, RD (2003) Development of Hepatozoon caimani (Carini, 1909) Pessôa, De Biasi & De Souza, 1972 in the Caiman Caiman c. crocodilus, the Frog Rana catesbeiana and the Mosquito Culex fatigans. Memórias do Instituto Oswaldo Cruz 98, 103–113.Google Scholar
Maia, JP, Alvares, F, Boratynski, Z, Brito, JC, Leite, JV and Harris, DJ (2014) Molecular assessment of Hepatozoon (apicomplexa: Adeleorina) infections in wild canids and rodents from North Africa, with implications for transmission dynamics across taxonomic groups. Journal of Wildlife Diseases 50, 837–848.Google Scholar
Mathew, JS, Van Den Bussche, RA, Ewing, SA, Malayer, JR, Latha, BR and Panciera, RJ (2000) Phylogenetic relationships of Hepatozoon (apicomplexa: Adeleorina) based on molecular, morphologic, and life cycle characters. Journal of Parasitology 86, 366–372.Google Scholar
Merino, S, Vásquez, RA, Martínez, J, Celis-Diez, JL, Gutiérrez-Jiménez, L, Ippi, S, Sánchez-Monsalvez, I and De la Puente, JM (2009) Molecular characterization of an ancient Hepatozoon species parasitizing the ‘living fossil’ marsupial ‘Monito del Monte’ Dromiciops gliroides from Chile. Biological Journal of the Linnean Society 98, 568–576.Google Scholar
Metzger, B, Paduan, KS, Rubini, AS, Oliveira, TG, Pereira, C and O'Dwyer, LH (2008) The first report of Hepatozoon sp. (Apicomplexa:Hepatozoidae) in Neotropical felids from Brazil. Veterinary Parasitology 152, 28–33.Google Scholar
Miller, WW (1908) Hepatozoon perniciosum (n. g., n. sp.); a haemogregarine pathogenic for white rats; with a description of the sexual cycle in the intermediate host, a mite (Lelaps echidninus). Hygienic Laboratory Bulletin 46, 51–123.Google Scholar
Netherlands, EC, Cook, CA, Du Preez, LH, Vanhove, MPM, Brendonck, L and Smit, NJ (2018) Monophyly of the species of Hepatozoon (adeleorina: Hepatozoidae) parasitizing (African) anurans, with the description of three new species from hyperoliid frogs in South Africa. Parasitology 145, 1039–1050.Google Scholar
Rigó, K, Majoros, G, Szekeres, S, Molnár, I, Jablonszky, M, Majláthová, V, Majláth, I and Foldvári, G (2016) Identification of Hepatozoon erhardovae Krampitz, 1964 from bank voles (Myodes glareolus) and fleas in Southern Hungary. Parasitology Research 115, 2409–2413.Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 1572–1574, Available at http://dx.doi.org/10.1093/bioinformatics/btg180.Google Scholar
Smith, TG (1996) The genus Hepatozoon (apicomplexa: Adeleina). Journal of Parasitology 82, 565–585.Google Scholar
Smith, TG, Desser, SS and Martin, DS (1994) The development of Hepatozoon sipedon sp. nov. (Apicomplexa: Adeleina: Hepatozoidae) in its natural host, the Northern water snake (Nerodia sipedon sipedon), in the culicine vectors, Culex pipiens and C. territans, and in an intermediate host, the Northern leopard frog (Rana pipiens). Parasitology Research 80, 559–568.Google Scholar
Sousa, KCM, Fernandes, MP, Herrera, HM, Benevenute, JL, Santos, FM, Rocha, FL, Barreto, WTG, Macedo, GC, Campos, JB, Martins, TF, de Andrade Pinto, PCE, Battesti, DB, Piranda, EM, Cançado, PHD, Machado, RZ and André, MR (2017) Molecular detection of Hepatozoon spp. in domestic dogs and wild mammals in southern Pantanal, Brazil with implications in the transmission route. Veterinary Parasitology 237, 37–46.Google Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Ujvari, B, Madsen, T and Olsson, M (2004) High prevalence Hepatozoon spp. (Apicomplexa, Hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia. Journal of Parasitology 90, 670–672.Google Scholar
Viana, LA, Soares, P, Silva, JE, Paiva, F and Coutinho, ME (2012) Anurans as paratenic hosts in the transmission of Hepatozoon caimani to caimans Caiman yacare and Caiman latirostris. Parasitology Research 110, 883–886.Google Scholar
Watkins, RA, Moshier, SE and Pinter, AJ (2006) The Flea, Megabothris abantis: an invertebrate host of Hepatozoon sp. and a likely definitive host in Hepatozoon infections of the Montane Vole, Microtus montanus. Journal of Wildlife Diseases 42, 386–390.Google Scholar
Wenyon, CM (1926) Protozoology Vol.1. New York, USA: William Wood and Company.Google Scholar
Wolf, RW, Aragona, M, Muñoz-Leal, S, Pinto, LB, Melo, ALT, Braga, IA, Costa, JS, Martins, TF, Marcili, A, Pacheco, RC, Labruna, MB and Aguiar, DM (2016) Novel Babesia and Hepatozoon agents infecting non-volant small mammals in the Brazilian Pantanal, with the first record of the tick Ornithodoros guaporensis in Brazil. Ticks and Tick-borne Diseases 7, 449–456.Google Scholar