{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,4]],"date-time":"2026-09-04T09:38:23Z","timestamp":1788514703999,"version":"build-2803163510"},"reference-count":24,"publisher":"Cambridge University Press (CUP)","issue":"9","license":[{"start":{"date-parts":[[2022,5,20]],"date-time":"2022-05-20T00:00:00Z","timestamp":1653004800000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/www.cambridge.org\/core\/terms"}],"content-domain":{"domain":["cambridge.org"],"crossmark-restriction":true},"short-container-title":["Parasitology"],"published-print":{"date-parts":[[2022,8]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>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 (<jats:italic>Bos taurus<\/jats:italic>), paired pyriforms (\u2018figure 8\u2019) of <jats:italic>Babesia divergens<\/jats:italic> are usual, but tetrads (\u2018Maltese Cross\u2019) 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 <jats:italic>B. divergens<\/jats:italic> 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 \u2018daisy head\u2019 (<jats:italic>vs<\/jats:italic> the usual 2, less often 4 merozoites). Reproduction is possible without egressing merozoites from the erythrocyte, which results in multi-occupancy of an RBC (\u22655 parasites per RBC). An unusually high polyparasitism \u2013 up to 14 parasites developed in the affected erythrocytes \u2013 was observed. This phenomenon is rare in natural hosts (usually \u22645), but when <jats:italic>B. divergens<\/jats:italic> is cultured <jats:italic>in vitro<\/jats:italic> it can be 10\u201312.<\/jats:p>","DOI":"10.1017\/s0031182022000439","type":"journal-article","created":{"date-parts":[[2022,5,20]],"date-time":"2022-05-20T05:23:45Z","timestamp":1653024225000},"page":"1160-1163","update-policy":"https:\/\/doi.org\/10.1017\/policypage","source":"Crossref","is-referenced-by-count":4,"title":["Extraordinary high level of propagation of <i>Babesia divergens<\/i> in severe human babesiosis"],"prefix":"10.1017","volume":"149","author":[{"given":"Irina V.","family":"Kukina","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5030-1691","authenticated-orcid":false,"given":"Olga P.","family":"Zelya","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"56","published-online":{"date-parts":[[2022,5,20]]},"reference":[{"key":"S0031182022000439_ref24","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1128\/CMR.16.4.622-636.2003","article-title":"Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance","volume":"16","author":"Zintl","year":"2003","journal-title":"Clinical Microbiology Reviews"},{"key":"S0031182022000439_ref4","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1007\/s10096-004-1270-x","article-title":"Role of quinine in life-threatening Babesia divergens infection successfully treated with clindamycin","volume":"24","author":"Corpelet","year":"2005","journal-title":"European Journal of Clinical Microbiology and Infectious Diseases"},{"key":"S0031182022000439_ref9","doi-asserted-by":"crossref","first-page":"1057","DOI":"10.1007\/s15010-013-0526-8","article-title":"Human babesiosis in Europe: what clinicians need to know","volume":"41","author":"Hildebrandt","year":"2013","journal-title":"Infection"},{"key":"S0031182022000439_ref10","doi-asserted-by":"crossref","unstructured":"Hildebrandt, A , Zintl, A , Montero, E , Hunfeld, K-P and Gray, J (2021) Human babesiosis in Europe pathogens 10, 1165.","DOI":"10.3390\/pathogens10091165"},{"key":"S0031182022000439_ref14","doi-asserted-by":"crossref","first-page":"e00414","DOI":"10.1016\/j.idcr.2018.e00414","article-title":"Fatal human babesiosis caused by Babesia divergens in an asplenic host","volume":"13","author":"Kukina","year":"2018","journal-title":"IDCases"},{"key":"S0031182022000439_ref7","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/BF00934377","article-title":"Cytological and immunological responses to Babesia divergens in different hosts: ox, gerbil, man","volume":"77","author":"Gorenflot","year":"1991","journal-title":"Parasitology Research"},{"key":"S0031182022000439_ref16","doi-asserted-by":"crossref","first-page":"114","DOI":"10.3201\/eid1701.100737","article-title":"Babesiosis in immunocompetent patients, Europe","volume":"17","author":"Martinot","year":"2011","journal-title":"Emerging Infectious Diseases"},{"key":"S0031182022000439_ref20","doi-asserted-by":"crossref","first-page":"14116","DOI":"10.1038\/s41598-018-32349-7","article-title":"Kinetics of the invasion and egress processes of Babesia divergens, observed by time-lapse video microscopy","volume":"8","author":"Sevilla","year":"2018","journal-title":"Scientific Reports"},{"key":"S0031182022000439_ref1","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1016\/j.ttbdis.2018.02.018","article-title":"A fatal case of Babesia divergens infection in Northwestern Spain","volume":"9","author":"Asensi","year":"2018","journal-title":"Ticks and Tick-Borne Diseases"},{"key":"S0031182022000439_ref11","doi-asserted-by":"crossref","first-page":"1219","DOI":"10.1016\/j.ijpara.2008.03.001","article-title":"Babesiosis: recent insights into an ancient disease","volume":"38","author":"Hunfeld","year":"2008","journal-title":"International Journal for Parasitology"},{"key":"S0031182022000439_ref22","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1645\/GE-662R.1","article-title":"In vitro host erythrocyte specificity and differential morphology of Babesia divergens and a zoonotic Babesia sp. from eastern cottontail rabbits (Sylvilagus floridanus)","volume":"92","author":"Spencer","year":"2006","journal-title":"Journal of Parasitology"},{"key":"S0031182022000439_ref15","doi-asserted-by":"crossref","first-page":"101262","DOI":"10.1016\/j.ttbdis.2019.07.006","article-title":"Severe babesiosis caused by Babesia divergens in a host with intact spleen, Russia, 2018","volume":"10","author":"Kukina","year":"2019","journal-title":"Ticks and Tick-Borne Diseases"},{"key":"S0031182022000439_ref23","first-page":"18","article-title":"Natural history of zoonotic Babesia: role of wildlife reservoirs","volume":"22","author":"Yabsley","year":"2013","journal-title":"International Journal for Parasitology: Parasites and Wildlife"},{"key":"S0031182022000439_ref18","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1016\/j.ttbdis.2017.02.016","article-title":"Splenic dysfunction from celiac disease resulting in severe babesiosis","volume":"8","author":"O'Connell","year":"2017","journal-title":"Ticks and Tick-Borne Diseases"},{"key":"S0031182022000439_ref17","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.ijid.2014.12.034","article-title":"Severe human Babesia divergens infection in Norway","volume":"33","author":"M\u00f8rch","year":"2015","journal-title":"International Journal of Infectious Diseases"},{"key":"S0031182022000439_ref2","doi-asserted-by":"crossref","first-page":"760","DOI":"10.1046\/j.1365-3156.2003.01074.x","article-title":"A fatal case of human babesiosis in Portugal: molecular and phylogenetic analysis","volume":"8","author":"Centeno-Lima","year":"2003","journal-title":"Tropical Medicine and International Health"},{"key":"S0031182022000439_ref3","doi-asserted-by":"crossref","DOI":"10.1128\/mSphere.00928-20","article-title":"Four-dimensional characterization of the Babesia divergens asexual life cycle, from the trophozoite to the multiparasite stage","volume":"5","author":"Conesa","year":"2020","journal-title":"mSphere"},{"key":"S0031182022000439_ref5","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1111\/cmi.12555","article-title":"Babesia divergens builds a complex population structure composed of specific ratios of infected cells to ensure a prompt response to changing environmental conditions","volume":"18","author":"Cursino-Santos","year":"2016","journal-title":"Cellular Microbiology"},{"key":"S0031182022000439_ref21","first-page":"11","article-title":"Piroplasmosis in man; report of a case","volume":"9","author":"Skrabalo","year":"1957","journal-title":"Documenta de medicina geographica et tropica"},{"key":"S0031182022000439_ref12","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1186\/s13071-016-1731-y","article-title":"Stimulation and quantification of Babesia divergens gametocytogenesis","volume":"9","author":"Jalovecka","year":"2016","journal-title":"Parasites and Vectors"},{"key":"S0031182022000439_ref6","doi-asserted-by":"crossref","first-page":"724","DOI":"10.3201\/eid2004.131409","article-title":"Severe babesiosis in immunocompetent man, Spain, 2011","volume":"20","author":"Gonzalez","year":"2014","journal-title":"Emerging Infectious Diseases"},{"key":"S0031182022000439_ref19","doi-asserted-by":"crossref","first-page":"e0003711","DOI":"10.1371\/journal.pntd.0003711","article-title":"Morphological and molecular descriptors of the developmental cycle of Babesia divergens parasites in human erythrocytes","volume":"9","author":"Rossouw","year":"2015","journal-title":"PLoS Neglected Tropical Diseases"},{"key":"S0031182022000439_ref8","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1146\/annurev-ento-011118-111932","article-title":"Vectors of babesiosis","volume":"64","author":"Gray","year":"2019","journal-title":"Annual Review of Entomology"},{"key":"S0031182022000439_ref13","volume-title":"Key to Protozoan Parasites (of Man, Domestic Animals and Agricultural Plants)","author":"Krylov","year":"1996"}],"container-title":["Parasitology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.cambridge.org\/core\/services\/aop-cambridge-core\/content\/view\/S0031182022000439","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,21]],"date-time":"2022-10-21T08:59:50Z","timestamp":1666342790000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.cambridge.org\/core\/product\/identifier\/S0031182022000439\/type\/journal_article"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,20]]},"references-count":24,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2022,8]]}},"alternative-id":["S0031182022000439"],"URL":"https:\/\/doi.org\/10.1017\/s0031182022000439","relation":{},"ISSN":["0031-1820","1469-8161"],"issn-type":[{"value":"0031-1820","type":"print"},{"value":"1469-8161","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,20]]},"assertion":[{"value":"Copyright \u00a9 The Author(s), 2022. Published by Cambridge University Press","name":"copyright","label":"Copyright","group":{"name":"copyright_and_licensing","label":"Copyright and Licensing"}}]}}