A new human opisthorchiasis outbreak in central Italy: a never-ending story.

Cholestasis Eosinophilia Opisthorchis Praziquantel Trematode Zoonosis

Journal

Infection
ISSN: 1439-0973
Titre abrégé: Infection
Pays: Germany
ID NLM: 0365307

Informations de publication

Date de publication:
26 Sep 2024
Historique:
received: 02 04 2024
accepted: 30 06 2024
medline: 26 9 2024
pubmed: 26 9 2024
entrez: 26 9 2024
Statut: aheadofprint

Résumé

Opisthorchis felineus is a trematode causing a foodborne infection transmitted by raw freshwater fish belonging to Cyprinidae family. Human outbreaks in Italy dated back to 2003-2011 and involved lakes of Central Italy. The aim of this study is to report epidemiological and clinical characteristics of the human opisthorchiasis outbreak occurred in Central Italy in 2022 comparing it with previous events. We report cases diagnosed from June to December 2022 in Perugia hospital thanks to serological and molecular tests and direct examination of feces. Sixty-seven individuals were traced back by epidemiological investigation. Forty-seven received a diagnosis of opisthorchiasis, of which 45 were confirmed cases and two were considered as probable cases. These 47 individuals attended a Trasimeno lakeshore restaurant in May 2022. All but 20 presented symptoms, mostly fever. Sixteen (15 confirmed and 1 probable) cases required hospitalization. Feces examination revealed Opisthorchis spp. eggs in 35/45 (78%) confirmed cases. Thirty individuals underwent to serology and molecular stool test: 5 (16.7%) results positive to the former, 1 (3.3%) to the latter while 4 (13.3%) to both. Laboratory tests, available in 28 patients, showed eosinophilia in 82.1%, increase of alanine aminotransferase, gamma-glutamyl transferase and alkaline phosphatase in 64.3%, 75% and 67.9%, respectively. Because of pharmacy shortage of praziquantel, 22 patients were treated with albendazole, of which 13 failed clearing the parasite. Opisthorchiasis still represents a challenging diagnosis, in particular for asymptomatic patients. Albendazole may lead to treatment failure. Control measures in known endemic areas should be implemented. number 27,498/23/ON, approved by Ethical Committee of Umbrian Region in 09.13.2023.

Identifiants

pubmed: 39325355
doi: 10.1007/s15010-024-02340-8
pii: 10.1007/s15010-024-02340-8
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

WHO. (1995) Control of foodborne trematodes infection. WHO Technical Report Series 849.
Pozio E, Armignacco O, Ferri F, Gómez-Morales MA. Opisthorchis Felineus, an emerging infection in Italy and its implication for the European Union. Acta Trop. 2013;126(1):54–62. https://doi.org/10.1016/j.actatropica.2013.01.005 .
doi: 10.1016/j.actatropica.2013.01.005 pubmed: 23337391
De Liberato C, Scaramozzino P, Brozzi A, Lorenzetti R, Di Cave D, Martini E, Lucangeli C, Pozio E, Berrilli F, Bossù T. Investigation on Opisthorchis felineus occurrence and life cycle in Italy. Vet Parasitol. 2011;177(1–2):67–71. https://doi.org/10.1016/j.vetpar.2010.11.042 .
doi: 10.1016/j.vetpar.2010.11.042 pubmed: 21168274
Crotti D, Crotti S. Opisthorchis felineus in deiezioni fecali della popolazione felina dell’Isola Maggiore Del Trasimeno (PG). Prog Vet. 2007;6:272–74.
Crotti D, D’Annibale ML, Crotti S. Opistorchiasi Autoctona Del Lago Trasimeno (Perugia): descrizione di due Episodi Epidemici Da Opisthorchis felineus e problematiche diagnostiche differenziali. Microbiol Med. 2007;22(1):36–41. https://doi.org/10.4081/mm.2007.2896 .
doi: 10.4081/mm.2007.2896
Pozio E, Gómez-Morales MA. Clonorchiasis and Opisthorchiasis. In: Bruschi F, editor. Helminth infections and their impact on global public health. Springer. 2022:221–56.
Pakharukova MY, Mordvinov VA. The liver fluke Opisthorchis felineus: biology, epidemiology and carcinogenic potential. Trans R Soc Trop Med Hyg. 2016;110:28–36. https://doi.org/10.1093/trstmh/trv085 .
doi: 10.1093/trstmh/trv085 pubmed: 26740360
Bouvard V, Baan R, Straif K, et al. A review of human carcinogens-part B: biological agents. Lancet Oncol. 2009;10:321–2. https://doi.org/10.1016/s1470-2045(09)70096-8 .
doi: 10.1016/s1470-2045(09)70096-8 pubmed: 19350698
Carcinogenic Hazards to Humans (IARC). List of classification. https://monographs.iarc.who.int/list-of-classifications/ [cited 2023 March 7].
Mordvinov VA, Yurlova NI, Ogorodova LM, Katokhin AV. Opisthorchis felineus and Metorchis bilis are the main agents of liver fluke infection of humans in Russia. Parasitol Int. 2012;61:25–31. https://doi.org/10.1016/j.parint.2011.07.021 .
doi: 10.1016/j.parint.2011.07.021 pubmed: 21840415
Maksimova GA, Pakharukova MY, Kashina EV, Zhukova NA, Kovner AV, Lvova MN, et al. Effect of Opisthorchis felineus infection and dimethylnitrosamine administration on the induction of cholangiocarcinoma in Syrian hamsters. Parasitol Int. 2017;66:458–63. https://doi.org/10.1016/j.parint.2015.10.002 .
doi: 10.1016/j.parint.2015.10.002 pubmed: 26453019
Kovner AV, Pakharukova MY, Maksimova GA, Mordvinov VA. Characteristics of liver fibrosis associated with chronic Opisthorchis felineus infection in Syrian hamsters and humans. Exp Mol Pathol. 2019;110:104274. https://doi.org/10.1016/j.yexmp.2019.104274 .
doi: 10.1016/j.yexmp.2019.104274 pubmed: 31226265
Lvova MN, Tangkawattana S, Balthaisong S, Katokhin AV, Mordvinov VA, Sripa B. Comparative histopathology of Opisthorchis Felineus and Opisthorchis viverrini in a hamster model: an implication of high pathogenicity of the European liver fluke. Parasitol Int. 2012;61:167–72. https://doi.org/10.1016/j.parint.2011.08.005 .
doi: 10.1016/j.parint.2011.08.005 pubmed: 21854870
Armignacco O, Ferri F, Gómez-Morales MA, Caterini L, Pozio E. Cryptic and asymptomatic Opisthorchis felineus infections. Am J Trop Med Hyg. 2013;88:364–66. https://doi.org/10.4269/ajtmh.2012.12-0280 .
doi: 10.4269/ajtmh.2012.12-0280 pubmed: 23249682 pmcid: 3583331
Müller B, Schmidt J, Mehlhorn H. PCR diagnosis of infections with different species of Opisthorchiidae using a rapid clean-up procedure for stool samples and specific primers. Parasitol Res. 2007;100:905–9. https://doi.org/10.1007/s00436-006-0321-x .
doi: 10.1007/s00436-006-0321-x pubmed: 17061114
Gómez-Morales MA, Ludovisi A, Amati M, Pozio E. Validation of an Excretory/Secretory Antigen based-Elisa for the diagnosis of Opisthorchis felineus infection in humans from low Trematode endemic areas. PLoS ONE. 2013;8(5):e62267. https://doi.org/10.1371/journal.pone.0062267 .
doi: 10.1371/journal.pone.0062267 pubmed: 23671589 pmcid: 3650035
Traverso A, Repetto E, Magnani S, Meloni T, Natrella M, Marchisio P, et al. A large outbreak of Opisthorchis felineus in Italy suggests that opisthorchiasis develops as a febrile eosinophilic syndrome with cholestasis rather than a hepatitis-like syndrome. Eur J Clin Microbiol Infect Dis. 2012;31(6):1089–93. https://doi.org/10.1007/s10096-011-1411-y .
doi: 10.1007/s10096-011-1411-y pubmed: 21938537
Vondeling AM, Lobatto S, Kortbeek LM, Naus H, Dorigo-Zetsma JW. Fever, malaise and eosinophilia after consumption of raw fish in Italy: infection by a liver fluke (Opisthorchis Felineus). Ned Tijdschr Geneeskd. 2012;156:A3873.
pubmed: 22296896
Wunderink HF, Rozemijer W, Wever PC, Verweij JJ, van Lieshout L. Foodborne Trematodiasis and Opisthorchis Felineus Acquired in Italy. Emerg Infect Dis. 2014;20(1):154–55. https://doi.org/10.3201/eid2001.130476 .
doi: 10.3201/eid2001.130476 pubmed: 24520562 pmcid: 3884715
Brugioni L, Tognetti M, Gozzi C. An unhealthy holiday on Lake Bolsena. Italian J Med. 2013;7(1):39–42. https://doi.org/10.4081/itjm.2013.39 .
doi: 10.4081/itjm.2013.39
Gustinelli A. Elminti di interesse zoonosico in specie ittiche dulciacquicole nazionali. Tesi di Dottorato in Epidemiologia e Controllo delle Zoonosi (ciclo XX), settore VET-06, Alma Mater Studiorum Bologna, http://amsdottorato.unibo.it/816/2/Gustinelli_Tesi_Dottorato_Epidemiologia_e_controllo_delle_zoonosi__XX_ciclo.pdf .
Cacciò SM, Chalmers RM, Dorny P, Robertson LJ. Foodborne parasites: outbreaks and outbreak investigations. A meeting report from the European network for foodborne parasites (Euro-FBP). Food Waterborne Parasitol. 2018;8(10):1–5. https://doi.org/10.1016/j.fawpar.2018.01.001 .
doi: 10.1016/j.fawpar.2018.01.001
Armignacco O, Caterini L, Marucci G, Ferri F, Bernardini G, Natalini Raponi G, et al. Human illnesses caused by Opisthorchis felineus flukes, Italy. Emerg Infect Dis. 2008;14(12):1902–5. https://doi.org/10.3201/eid1412.080782 .
doi: 10.3201/eid1412.080782 pubmed: 19046516 pmcid: 2634636
Ponomareva NM, Orlova TV, Vlasenko PG, Serbina EA, Yurlova NI. Temperature dependence of Opisthorchis felineus infection in the first intermediate host snail, Bithynia Troschelii. Acta Trop. 2024;253:107166. https://doi.org/10.1016/j.actatropica.2024.107166 .
doi: 10.1016/j.actatropica.2024.107166 pubmed: 38431135
Sithithaworn P, Andrews RH, Mordvinov VA, Pakharukova MY, Lvova MN. Opisthorchis viverrini and Opisthorchis Felineus. Encyclopedia of Food Safety. Academic; 2024. pp. 673–68.
European Food Safety Authority. Scientific opinion on risk assessment of parasites in fishery products. EFSA J. 2010;8:1543. https://doi.org/10.2903/j.efsa.2010.1543 .
doi: 10.2903/j.efsa.2010.1543

Auteurs

Chiara Papalini (C)

Infectious Diseases Clinic, Santa Maria della Misericordia Hospital, University of Perugia, Piazzale Gambuli 1, Perugia, 06100, Italy. chiara.papalini@ospedale.perugia.it.

Maria Angeles Gómez-Morales (MA)

Department of Infectious Diseases, European Union Reference Laboratory for Parasites, Istituto Superiore di Sanità, Roma, Italy.

Alessandra Mercuri (A)

Infectious Diseases Clinic, Santa Maria della Misericordia Hospital, University of Perugia, Piazzale Gambuli 1, Perugia, 06100, Italy.

Elisa Stolaj (E)

Infectious Diseases Clinic, Santa Maria della Misericordia Hospital, University of Perugia, Piazzale Gambuli 1, Perugia, 06100, Italy.

Maria Grazia Brancaleoni (MG)

Department of Prevention, Travel Medicine Unit, Local Health Unit Umbria 1, Perugia, Italy.

Igino Fusco Moffa (I)

Department of Prevention, Travel Medicine Unit, Local Health Unit Umbria 1, Perugia, Italy.

Giovanni Lo Vaglio (G)

Department of Prevention, Hygiene of food of animal origin, Local Health Unit Umbria 1, Trasimeno area, Panicale, Perugia, Italy.

Alessandra Ludovisi (A)

Department of Infectious Diseases, European Union Reference Laboratory for Parasites, Istituto Superiore di Sanità, Roma, Italy.

Gianluca Marucci (G)

Department of Infectious Diseases, European Union Reference Laboratory for Parasites, Istituto Superiore di Sanità, Roma, Italy.

Daniela Francisci (D)

Infectious Diseases Clinic, Santa Maria della Misericordia Hospital, University of Perugia, Piazzale Gambuli 1, Perugia, 06100, Italy.

Classifications MeSH