Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-17T10:14:14.255Z Has data issue: false hasContentIssue false
  • English
  • Français

Extraordinary high level of propagation of Babesia divergens in severe human babesiosis

Published online by Cambridge University Press:  20 May 2022

Irina V. Kukina  and
Olga P. Zelya Open the ORCID record for Olga P. Zelya [Opens in a new window]
Irina V. Kukina
Affiliation:
Martsinovsky Institute of Medical Parasitology, Tropical and Vector-Borne Diseases, Sechenov University, Moscow, Russia
Olga P. Zelya*
Affiliation:
Martsinovsky Institute of Medical Parasitology, Tropical and Vector-Borne Diseases, Sechenov University, Moscow, Russia
*
Author for correspondence: Olga P. Zelya, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Babesias are obligate apicomplexan parasites that affect the red blood cells (RBCs) of animals. Humans can serve as accidental hosts for them. Asexual reproduction of a parasite occurs in a vertebrate host through asynchronous binary fission, yielding a complex pleomorphic population of intraerythrocytic forms. In natural hosts (Bos taurus), paired pyriforms (‘figure 8’) of Babesia divergens are usual, but tetrads (‘Maltese Cross’) are very rare (only in 0.02% infected erythrocytes); in humans, however, up to 5% of infected erythrocytes show tetrads. The current study shows that B. divergens proliferating in an accidental human host can promote extraordinarily high level of fission. This phenomenon is expressed as the simultaneous division of the parasite into 6 and possibly a greater number of merozoites, forming a ‘daisy head’ (vs the usual 2, less often 4 merozoites). Reproduction is possible without egressing merozoites from the erythrocyte, which results in multi-occupancy of an RBC (≥5 parasites per RBC). An unusually high polyparasitism – up to 14 parasites developed in the affected erythrocytes – was observed. This phenomenon is rare in natural hosts (usually ≤5), but when B. divergens is cultured in vitro it can be 10–12.

Keywords

asexual reproductionBabesia divergenshuman babesiosismulti-occupancy of an RBC
Type
Research Article
Information
Parasitology , Volume 149 , Issue 9 , August 2022 , pp. 1160 - 1163
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

Asensi, V, González, LM, Fernández-Suárez, J, Sevilla, E, Navascués, RÁ, Suárez, ML, Lauret, ME, Bernardo, A, Carton, JA and Montero, E (2018) A fatal case of Babesia divergens infection in Northwestern Spain. Ticks and Tick-Borne Diseases 9, 730–734.CrossRefGoogle ScholarPubMed
Centeno-Lima, S, do Rosário, V, Parreira, R, Maia, AJ, Freudenthal, AM, Nijhof, AM and Jongejan, F (2003) A fatal case of human babesiosis in Portugal: molecular and phylogenetic analysis. Tropical Medicine and International Health 8, 760–764.CrossRefGoogle ScholarPubMed
Conesa, JJ, Sevilla, E, Terrón, MC, González, LM, Gray, J, Pérez-Berná, AJ, Carrascosa, JL, Pereiro, E, Chichón, FJ, Luque, D and Montero, E (2020) Four-dimensional characterization of the Babesia divergens asexual life cycle, from the trophozoite to the multiparasite stage. mSphere 5, e00928-20.CrossRefGoogle Scholar
Corpelet, C, Vacher, P, Coudore, F, Laurichesse, H, Conort, N and Souweine, B (2005) Role of quinine in life-threatening Babesia divergens infection successfully treated with clindamycin. European Journal of Clinical Microbiology and Infectious Diseases 24, 74–75.CrossRefGoogle ScholarPubMed
Cursino-Santos, JR, Singh, M, Pham, P, Rodriguez, M and Lobo, CA (2016) Babesia divergens builds a complex population structure composed of specific ratios of infected cells to ensure a prompt response to changing environmental conditions. Cellular Microbiology 18, 859–874.CrossRefGoogle ScholarPubMed
Gonzalez, LM, Rojo, S, Gonzalez-Camacho, F, Luque, D, Lobo, CA and Montero, E (2014) Severe babesiosis in immunocompetent man, Spain, 2011. Emerging Infectious Diseases 20, 724–726.CrossRefGoogle Scholar
Gorenflot, A, Brasseur, P, Precigout, E, L'Hostis, M, Marchand, A and Schrevel, J (1991) Cytological and immunological responses to Babesia divergens in different hosts: ox, gerbil, man. Parasitology Research 77, 3–12.CrossRefGoogle ScholarPubMed
Gray, JS, Estrada-Peña, A and Zintl, A (2019) Vectors of babesiosis. Annual Review of Entomology 64, 149–165.CrossRefGoogle ScholarPubMed
Hildebrandt, A, Gray, JS and Hunfeld, K-P (2013) Human babesiosis in Europe: what clinicians need to know. Infection 41, 1057–1072.CrossRefGoogle ScholarPubMed
Hildebrandt, A, Zintl, A, Montero, E, Hunfeld, K-P and Gray, J (2021) Human babesiosis in Europe pathogens 10, 1165.CrossRefGoogle Scholar
Hunfeld, K-P, Hildebrandt, A and Gray, JS (2008) Babesiosis: recent insights into an ancient disease. International Journal for Parasitology 38, 1219–1237.CrossRefGoogle ScholarPubMed
Jalovecka, M, Bonsergent, C, Hajdusek, O, Kopacek, P and Malandrin, L (2016) Stimulation and quantification of Babesia divergens gametocytogenesis. Parasites and Vectors 9, 439.CrossRefGoogle ScholarPubMed
Krylov, MV (1996) Key to Protozoan Parasites (of Man, Domestic Animals and Agricultural Plants). St. Petersburg: Russian Academy of Sciences. Zoological Institute.Google Scholar
Kukina, IV, Guzeeva, TM, Zelya, OP and Ganushkina, LA (2018) Fatal human babesiosis caused by Babesia divergens in an asplenic host. IDCases 13, e00414.CrossRefGoogle Scholar
Kukina, IV, Zelya, OP, Guzeeva, TM, Karan, LS, Perkovskaya, IA, Tymoshenko, NI and Guzeeva, MV (2019) Severe babesiosis caused by Babesia divergens in a host with intact spleen, Russia, 2018. Ticks and Tick-Borne Diseases 10, 101262.CrossRefGoogle Scholar
Martinot, M, Zadeh, MM, Hansmann, Y, Grawey, I, Christmann, D, Aguillon, S, Jouglin, M, Chauvin, A and DeBriel, D (2011) Babesiosis in immunocompetent patients, Europe. Emerging Infectious Diseases 17, 114–116.CrossRefGoogle ScholarPubMed
Mørch, K, Holmaas, G, Frolander, PS and Kristoffersen, EK (2015) Severe human Babesia divergens infection in Norway. International Journal of Infectious Diseases 33, 37–38.CrossRefGoogle ScholarPubMed
O'Connell, S, Lyons, C, Abdou, M, Patowary, R, Aslam, S, Kinsella, N, Zintl, A, Hunfeld, K-P, Wormser, GP, Gray, J, Merry, C and Alizadeh, H (2017) Splenic dysfunction from celiac disease resulting in severe babesiosis. Ticks and Tick-Borne Diseases 8, 537–539.CrossRefGoogle ScholarPubMed
Rossouw, I, Maritz-Olivier, C, Niemand, J, van Biljon, R, Smit, A, Olivier, NA and Birkholtz, L-M (2015) Morphological and molecular descriptors of the developmental cycle of Babesia divergens parasites in human erythrocytes. PLoS Neglected Tropical Diseases 9, e0003711.CrossRefGoogle ScholarPubMed
Sevilla, E, González, LM, Luque, D, Gray, J and Montero, E (2018) Kinetics of the invasion and egress processes of Babesia divergens, observed by time-lapse video microscopy. Scientific Reports 8, 14116.CrossRefGoogle ScholarPubMed
Skrabalo, Z and Deanovic, Z (1957) Piroplasmosis in man; report of a case. Documenta de medicina geographica et tropica 9, 11–16.Google ScholarPubMed
Spencer, AM, Goethert, HK, Telford, SR 3rd and Holman, PJ (2006) In vitro host erythrocyte specificity and differential morphology of Babesia divergens and a zoonotic Babesia sp. from eastern cottontail rabbits (Sylvilagus floridanus). Journal of Parasitology 92, 333–340.CrossRefGoogle Scholar
Yabsley, MJ and Shock, BC (2013) Natural history of zoonotic Babesia: role of wildlife reservoirs. International Journal for Parasitology: Parasites and Wildlife 22, 18–31.Google Scholar
Zintl, A, Mulcahy, G, Skerrett, HE, Taylor, SM and Gray, J (2003) Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clinical Microbiology Reviews 16, 622–636.CrossRefGoogle ScholarPubMed