{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:54:14Z","timestamp":1760144054153,"version":"build-2065373602"},"reference-count":29,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2024,3,18]],"date-time":"2024-03-18T00:00:00Z","timestamp":1710720000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"EU funding within the MUR PNRR Extended Partnership initiative on Emerging Infectious Diseases","award":["PE00000007, INF-ACT"],"award-info":[{"award-number":["PE00000007, INF-ACT"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Medicina"],"abstract":"<jats:p>Background and Objectives: the principal purpose of this literature review is to cluster adults with hematological malignancies after treatment or on maintenance with obinutuzumab who experienced disseminated EV infection to understand clinical characteristics and outcome of this rare condition in these patients. We report the first clinical case of a male affected by follicular lymphoma treated with immune-chemotherapy including obinutuzumab who was affected by disseminated EV infection with cardiovascular involvement. Materials and Methods: this narrative review summarizes all the research about disseminated EV infection in immunosuppressed adult patients treated with obinutuzumab from January 2000 to January 2024 using the Scale for the Assessment of Narrative Review Articles (SANRA) flow-chart. We performed a descriptive statistic using the standard statistical measures for quantitative data. Results: we included six studies, five case reports, and one case report with literature analysis. We collected a total of seven patients, all female, with disseminated EV infection. The most common signs and clinical presentations of EV infection were fever and encephalitis symptoms (N = 6, 85.7%), followed by hepatitis\/acute liver failure (N = 5, 71.4%). Conclusions: onco-hematological patients who receive immune-chemotherapy with a combination of treatments which depress adaptative immunity, which includes the antiCD20 obinutuzumab, could be at higher risk of disseminated EV infection, including CNS and cardiac involvement.<\/jats:p>","DOI":"10.3390\/medicina60030495","type":"journal-article","created":{"date-parts":[[2024,3,18]],"date-time":"2024-03-18T06:58:39Z","timestamp":1710745119000},"page":"495","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Disseminated Enterovirus Infection in a Patient Affected by Follicular Lymphoma Treated with Obinutuzumab: A Case Report and a Narrative Review of the Literature"],"prefix":"10.3390","volume":"60","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3865-9519","authenticated-orcid":false,"given":"Tommaso","family":"Lupia","sequence":"first","affiliation":[{"name":"Unit of Infectious Diseases, AOU City of Health and Sciences, 10100 Turin, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Silvia","family":"Corcione","sequence":"additional","affiliation":[{"name":"Unit of Infectious Diseases, AOU City of Health and Sciences, 10100 Turin, Italy"},{"name":"Department of Medical Sciences, Infectious Diseases, University of Turin, 10126 Turin, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elena","family":"Staffilano","sequence":"additional","affiliation":[{"name":"Department of Medical Sciences, Infectious Diseases, University of Turin, 10126 Turin, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roberta","family":"Bosio","sequence":"additional","affiliation":[{"name":"Department of Medical Sciences, Infectious Diseases, University of Turin, 10126 Turin, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8101-4196","authenticated-orcid":false,"given":"Antonio","family":"Curtoni","sequence":"additional","affiliation":[{"name":"Microbiology and Virology Unit, AOU City of Health and Sciences, 10100 Turin, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5361-5613","authenticated-orcid":false,"given":"Alessandro","family":"Busca","sequence":"additional","affiliation":[{"name":"Department of Oncology, Stem Cell Transplant Center, Citt\u00e0 Della Salute e Della Scienza Hospital, 10100 Turin, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8338-0130","authenticated-orcid":false,"given":"Francesco Giuseppe","family":"De Rosa","sequence":"additional","affiliation":[{"name":"Unit of Infectious Diseases, AOU City of Health and Sciences, 10100 Turin, Italy"},{"name":"Department of Medical Sciences, Infectious Diseases, University of Turin, 10126 Turin, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,3,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Committee on the Enteroviruses, and National Foundation for Infantile Paralysis (1957). The Enteroviruses. Am. J. Public Health Nations Health, 47, 1556\u20131566.","DOI":"10.2105\/AJPH.47.12.1556"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1038\/s41579-018-0005-4","article-title":"The life cycle of non-polio enteroviruses and how to target it","volume":"16","author":"Baggen","year":"2018","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"297","DOI":"10.5005\/jp-journals-11002-0036","article-title":"Enteroviral Infections in Infants","volume":"1","author":"Maheshwari","year":"2022","journal-title":"Newborn"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/B978-0-444-53488-0.00018-3","article-title":"Enterovirus\/Picornavirus infections","volume":"Volume 123","author":"Jubelt","year":"2014","journal-title":"Handbook of Clinical Neurology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1007\/BF00918150","article-title":"Chronic enteroviral meningoencephalitis in agammaglobulinemia: Case report and literature review","volume":"12","author":"Misbah","year":"1992","journal-title":"J. Clin. Immunol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1038\/s41572-019-0132-x","article-title":"Follicular lymphoma","volume":"5","author":"Carbone","year":"2019","journal-title":"Nat. Rev. Dis. Prim."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s41073-019-0064-8","article-title":"SANRA\u2014A scale for the quality assessment of narrative review articles","volume":"26","author":"Baethge","year":"2019","journal-title":"Res. Integr. Peer Rev."},{"key":"ref_8","unstructured":"Li, W. (2022). Leukemia, Exon Publications."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/ejh.13278","article-title":"Fatal disseminated enterovirus infection in a patient with follicular lymphoma undergoing obinutuzumab maintenance therapy","volume":"103","author":"Heger","year":"2019","journal-title":"Eur. J. Haematol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1661","DOI":"10.3201\/eid2109.150104","article-title":"Disseminated Enteroviral Infection Associated with Obinutuzumab","volume":"21","author":"Dendle","year":"2015","journal-title":"Emerg. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"913","DOI":"10.3201\/eid2005.131766","article-title":"Coxsackievirus A16 Encephalitis during Obinutuzumab Therapy, Belgium, 2013","volume":"20","author":"Eyckmans","year":"2014","journal-title":"Emerg. Infect. Dis."},{"key":"ref_12","unstructured":"Blau, B.J., and Bass, A.R. (2024, February 10). Chronic Enterovirus Infection Manifesting as Diffuse Myalgias and Arthralgias in a 67-Year-Old Woman Receiving Obinutuzumab. Grand Rounds from HSS: Management of Complex Cases, 2023, Volume 12, Issue 3. Available online: https:\/\/www.hss.edu\/conditions_complexcase-chronic-enterovirus-infection.asp."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.ijid.2021.10.002","article-title":"Characteristics and therapy of enteroviral encephalitis: Case report and systematic literature review","volume":"113","author":"Wagner","year":"2021","journal-title":"Int. J. Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1002\/jmv.27370","article-title":"Disseminated enterovirus infection in a patient treated with obinutuzumab","volume":"94","author":"McNeil","year":"2022","journal-title":"J. Med. Virol."},{"key":"ref_15","unstructured":"(2024, February 10). Available online: https:\/\/fda-approves-gazyva-chronic-lymphocytic-leukemia-3955.html."},{"key":"ref_16","unstructured":"(2024, February 10). Available online: https:\/\/www.ema.europa.eu\/en\/medicines\/human\/orphan-designations\/eu-3-12-1054."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1331","DOI":"10.1056\/NEJMoa1614598","article-title":"Obinutuzumab for the First-Line Treatment of Follicular Lymphoma","volume":"377","author":"Marcus","year":"2017","journal-title":"N. Engl. J. Med."},{"key":"ref_18","unstructured":"Khetsuriani, N., Lamonte-Fowlkes, A., Oberst, S., Pallansch, M.A., and Centers for Disease Control and Prevention (2002). Enterovirus Surveillance\u2013United States, 1970\u20132005. Morbidity and Mortality Weekly Report. Surveillance Summaries, Centers for Disease Control and Prevention."},{"key":"ref_19","first-page":"1615","article-title":"Enteroviruses: Classification, diseases they cause, and approaches to development of antiviral drugs","volume":"82","author":"Nikonov","year":"2017","journal-title":"Biochemistry"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1002\/hon.2365","article-title":"Enteroviral infection in patients treated with rituximab for non-Hodgkin lymphoma: A case series and review of the literature","volume":"35","author":"Grisariu","year":"2017","journal-title":"Hematol. Oncol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1128\/microbiolspec.DMIH2-0006-2015","article-title":"Enteroviruses and Parechoviruses","volume":"4","author":"Dunn","year":"2016","journal-title":"Microbiol. Spectr."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3026","DOI":"10.1007\/s00415-020-10265-z","article-title":"An overview of viral infections of the nervous system in the immunosuppressed","volume":"268","author":"Kennedy","year":"2021","journal-title":"J. Neurol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"512","DOI":"10.3109\/10428194.2015.1110748","article-title":"Bendamustine associated immune suppression and infections during therapy of hematological malignancies","volume":"57","author":"Polliack","year":"2016","journal-title":"Leuk. Lymphoma"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1002\/hon.2828","article-title":"Obinutuzumab-related adverse events: A systematic review and meta-analysis","volume":"39","author":"Amitai","year":"2021","journal-title":"Hematol. Oncol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.jaci.2010.04.016","article-title":"Recurrent and persistent respiratory tract viral infections in patients with primary hypogammaglobulinemia","volume":"126","author":"Kainulainen","year":"2010","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Li, Y., Liu, M., Yan, Y., Wang, Z., Dai, Q., Yang, X., Guo, X., Li, W., Chen, X., and Cao, R. (2022). Molnupiravir and Its Active Form, EIDD-1931, Show Potent Antiviral Activity against Enterovirus Infections In Vitro and In Vivo. Viruses, 14.","DOI":"10.3390\/v14061142"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1007\/s13365-021-01038-z","article-title":"Compassionate-use pocapavir and immunoglobulin therapy for treatment of rituximab-associated enterovirus meningoencephalitis","volume":"28","author":"Epstein","year":"2022","journal-title":"J. Neurovirol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"bcr2017224133","DOI":"10.1136\/bcr-2017-224133","article-title":"Successful treatment of fulminant neonatal enteroviral myocarditis in monochorionic diamniotic twins with cardiopulmonary support, intravenous immunoglobulin and pocapavir","volume":"2018","author":"Amdani","year":"2018","journal-title":"BMJ Case Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"804","DOI":"10.1016\/S0140-6736(89)92270-8","article-title":"Chronic relapsing pericarditis and dilated cardiomyopathy: Serological evidence of persistent enterovirus infection","volume":"333","author":"Muir","year":"1989","journal-title":"Lancet"}],"container-title":["Medicina"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1648-9144\/60\/3\/495\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:15:08Z","timestamp":1760105708000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1648-9144\/60\/3\/495"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,18]]},"references-count":29,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2024,3]]}},"alternative-id":["medicina60030495"],"URL":"https:\/\/doi.org\/10.3390\/medicina60030495","relation":{},"ISSN":["1648-9144"],"issn-type":[{"type":"electronic","value":"1648-9144"}],"subject":[],"published":{"date-parts":[[2024,3,18]]}}}