Literature DB >> 31625839

Secondary Autochthonous Outbreak of Chikungunya, Southern Italy, 2017.

Flavia Riccardo, Giulietta Venturi, Marco Di Luca, Martina Del Manso, Francesco Severini, Xanthi Andrianou, Claudia Fortuna, Maria Elena Remoli, Eleonora Benedetti, Maria Grazia Caporali, Francesca Fratto, Anna Domenica Mignuoli, Liliana Rizzo, Giuseppe De Vito, Vincenzo De Giorgio, Lorenzo Surace, Francesco Vairo, Paola Angelini, Maria Carla Re, Antonello Amendola, Cristiano Fiorentini, Giulia Marsili, Luciano Toma, Daniela Boccolini, Roberto Romi, Patrizio Pezzotti, Giovanni Rezza, Caterina Rizzo.   

Abstract

In 2017, a chikungunya outbreak in central Italy later evolved into a secondary cluster in southern Italy, providing evidence of disease emergence in new areas. Officials have taken action to raise awareness among clinicians and the general population, increase timely case detection, reduce mosquito breeding sites, and promote mosquito bite prevention.

Entities:  

Keywords:  CHIKV; Calabria; Chikungunya; Italy; autochthonous; chikungunya virus; outbreak; viruses

Mesh:

Year:  2019        PMID: 31625839      PMCID: PMC6810187          DOI: 10.3201/eid2511.180949

Source DB:  PubMed          Journal:  Emerg Infect Dis        ISSN: 1080-6040            Impact factor:   6.883


In 2007 () and 2017 (), local outbreaks of human chikungunya infection occurred in Italy; both outbreaks were caused by the East/Central/South African strain of chikungunya virus (CHIKV). Both outbreaks were sustained by the invasive mosquito Aedes albopictus, largely established in Italy and other countries in southern Europe (). In 2017, France and Italy reported local transmission of CHIKV (,). However, in France, the number of cases was limited; whereas in Italy, 499 probable and confirmed cases of locally acquired CHIKV infection occurred, of which 270 were laboratory confirmed as per the European Union (EU) case definition of June 22, 2018 (https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32018D0945&from=EN#page=13). After local CHIKV transmission was confirmed in the seaside city of Anzio (Lazio region, central Italy) in 2017, the outbreak spread within the region, including in the city of Rome (–). The beginning of the outbreak was traced back to June 2017 (Figure 1). Subsequently, an outbreak developed in Guardavalle Marina, a small village of 2,346 inhabitants in the Calabria region of southern Italy, causing 100 probable/confirmed cases (Figures 1, 2).
Figure 1

Epidemic curve for 499 cases of chikungunya (probable and confirmed) in central and southern Italy, June 26–November 15, 2017.

Figure 2

Location and size of clusters of 499 cases of chikungunya (probable and confirmed), by municipality, in central and southern Italy, June 26–November 15, 2017.

Epidemic curve for 499 cases of chikungunya (probable and confirmed) in central and southern Italy, June 26–November 15, 2017. Location and size of clusters of 499 cases of chikungunya (probable and confirmed), by municipality, in central and southern Italy, June 26–November 15, 2017.

The Cases

In August 2017, a patient from Anzio arrived in Guardavalle Marina the day before onset of symptoms that met the clinical criteria of the EU case definition for chikungunya (suspected case); subsequently, more cases in the village were reported. For most case-patients, the clinical course of the disease was fairly mild. All patients with confirmed/probable cases reported fever, and 99% reported severe and persistent joint pain, which seemed to be the most indicative symptom of chikungunya (Appendix Table 2). Phylogenetic analysis of isolates from patients with confirmed cases and from mosquito pools showed that the virus strains from Lazio and Calabria were similar to the East/Central/South African strains detected in Pakistan and India (,). Neither strain contained the A226V mutation that was detected in the strain responsible for the 2007 outbreak in Italy (). The epidemiologic and microbiological evidence (Appendix) supports the hypothesis that the Guardavalle Marina outbreak originated from Lazio rather than from an independent introduction. The overall clinically observed attack rate in Guardavalle Marina was 4.3%, similar to the 5.4% rate reported during the 2007 outbreak in Castiglione di Cervia but much lower than the 34% rate reported in La Réunion () or the high attack rates typically reported by other affected tropical countries (). The duration of the Guardavalle Marina outbreak (2 months) was also closer to the duration of the outbreak in Castiglione di Cervia (July–September 2007) than to the duration of the outbreak in La Réunion (March 2005–April 2006) (). Clinically observed attack rates progressively increased with patient age (Appendix Table 1). This pattern was also observed during the 2007 outbreak in Italy () and was mainly attributed to older age being a proxy for specific behavior linked to higher exposure to bites from Ae. albopictus mosquitoes (). We cannot exclude underestimation of the observed attack rate in Guardavalle Marina, even though extensive door-to-door case finding was feasible and performed, given the small size of the village. Notwithstanding the lack of the A226V mutation, the 2017 strain was introduced and rapidly spread with evidence of disease emergence in new areas. Statistically significant case clustering was confirmed by spatiotemporal data analysis in Guardavalle Marina (Appendix Figure 2), and Ae. albopictus mosquito vector competence for the 2017 strain was recently found to be comparable to competence for the 2007 mutated strain (). Delayed clinical detection of cases, possibly resulting from lack of CHIKV infection awareness among clinicians (), and hence delayed testing for laboratory confirmation, could explain the size and extension of the 2017 outbreak. The fact that the outbreak was contained in a relatively short time after detection could be the result of the combination of targeted vector control interventions (Appendix), cooling temperatures, and increased rainfall during October–November 2017.

Conclusions

Since 2011, Italy has had a yearly updated plan for the surveillance and control of human infections caused by CHIKV; the plan includes designated reference laboratories, vector control, and blood/transplant safety measures (Appendix). After the 2017 outbreak, a “presumed local cluster” was defined as occurring when local transmission of CHIKV is suspected for >2 cases, of which only 1 case needs to be laboratory confirmed. It is sufficient for the second case to be suspected on clinical and epidemiologic grounds pending laboratory confirmation. This new definition, aimed at triggering more timely blood/transplant safety and outbreak response measures, was successfully implemented in 2018. Actions to raise awareness among clinicians and the general population are being designed as part of a joint effort of animal and human public health institutions and universities coordinated by the Italy Ministry of Health. These actions are aimed at increasing timely case detection, reducing the number of mosquito breeding sites, and promoting individual prevention of mosquito bites.

Appendix

Additional methods and results for study of secondary autochthonous outbreak of chikungunya, southern Italy, 2017.
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1.  Chikungunya virus in North-Eastern Italy: a seroprevalence survey.

Authors:  Maria Luisa Moro; Carlo Gagliotti; Giuliano Silvi; Raffaella Angelini; Vittorio Sambri; Giovanni Rezza; Erika Massimiliani; Andrea Mattivi; Elisa Grilli; Alba Carola Finarelli; Nadir Spataro; Anna Maria Pierro; Thomas Seyler; Pierluigi Macini
Journal:  Am J Trop Med Hyg       Date:  2010-03       Impact factor: 2.345

Review 2.  Chikungunya fever: an epidemiological review of a re-emerging infectious disease.

Authors:  J Erin Staples; Robert F Breiman; Ann M Powers
Journal:  Clin Infect Dis       Date:  2009-09-15       Impact factor: 9.079

3.  [Epidemiological surveillance du chikungunya on Reunion Island from 2005 to 2011].

Authors:  S Larrieu; E Balleydier; Ph Renault; M Baville; L Filleul
Journal:  Med Trop (Mars)       Date:  2012-03

4.  Infection with chikungunya virus in Italy: an outbreak in a temperate region.

Authors:  G Rezza; L Nicoletti; R Angelini; R Romi; A C Finarelli; M Panning; P Cordioli; C Fortuna; S Boros; F Magurano; G Silvi; P Angelini; M Dottori; M G Ciufolini; G C Majori; A Cassone
Journal:  Lancet       Date:  2007-12-01       Impact factor: 79.321

5.  Chikungunya disease outbreak, Reunion Island.

Authors:  Loïc Josseran; Christophe Paquet; Abdelkrim Zehgnoun; Nadège Caillere; Alain Le Tertre; Jean-Louis Solet; Martine Ledrans
Journal:  Emerg Infect Dis       Date:  2006-12       Impact factor: 6.883

6.  Vector competence of Aedes albopictus for the Indian Ocean lineage (IOL) chikungunya viruses of the 2007 and 2017 outbreaks in Italy: a comparison between strains with and without the E1:A226V mutation.

Authors:  Claudia Fortuna; Luciano Toma; Maria Elena Remoli; Antonello Amendola; Francesco Severini; Daniela Boccolini; Roberto Romi; Giulietta Venturi; Giovanni Rezza; Marco Di Luca
Journal:  Euro Surveill       Date:  2018-05

7.  Local transmission of chikungunya in Rome and the Lazio region, Italy.

Authors:  Francesco Vairo; Alessia Mammone; Simone Lanini; Emanuele Nicastri; Concetta Castilletti; Fabrizio Carletti; Vincenzo Puro; Domenico Di Lallo; Vincenzo Panella; Donatella Varrenti; Paola Scaramozzino; Antonino di Caro; Paola Scognamiglio; Maria Rosaria Capobianchi; Giuseppe Ippolito
Journal:  PLoS One       Date:  2018-12-21       Impact factor: 3.240

8.  Preliminary report of an autochthonous chikungunya outbreak in France, July to September 2017.

Authors:  Clémentine Calba; Mathilde Guerbois-Galla; Florian Franke; Charles Jeannin; Michelle Auzet-Caillaud; Gilda Grard; Lucette Pigaglio; Anne Decoppet; Joel Weicherding; Marie-Christine Savaill; Manuel Munoz-Riviero; Pascal Chaud; Bernard Cadiou; Lauriane Ramalli; Pierre Fournier; Harold Noël; Xavier De Lamballerie; Marie-Claire Paty; Isabelle Leparc-Goffart
Journal:  Euro Surveill       Date:  2017-09

9.  Detection of a chikungunya outbreak in Central Italy, August to September 2017.

Authors:  Giulietta Venturi; Marco Di Luca; Claudia Fortuna; Maria Elena Remoli; Flavia Riccardo; Francesco Severini; Luciano Toma; Martina Del Manso; Eleonora Benedetti; Maria Grazia Caporali; Antonello Amendola; Cristiano Fiorentini; Claudio De Liberato; Roberto Giammattei; Roberto Romi; Patrizio Pezzotti; Giovanni Rezza; Caterina Rizzo
Journal:  Euro Surveill       Date:  2017-09

10.  Transmission dynamics of the ongoing chikungunya outbreak in Central Italy: from coastal areas to the metropolitan city of Rome, summer 2017.

Authors:  Mattia Manica; Giorgio Guzzetta; Piero Poletti; Federico Filipponi; Angelo Solimini; Beniamino Caputo; Alessandra Della Torre; Roberto Rosà; Stefano Merler
Journal:  Euro Surveill       Date:  2017-11
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Review 1.  A comparative analysis of the 2007 and 2017 Italian chikungunya outbreaks and implication for public health response.

Authors:  Beniamino Caputo; Gianluca Russo; Mattia Manica; Francesco Vairo; Piero Poletti; Giorgio Guzzetta; Stefano Merler; Carolina Scagnolari; Angelo Solimini
Journal:  PLoS Negl Trop Dis       Date:  2020-06-11

2.  Chikungunya virus infections in Finnish travellers 2009-2019.

Authors:  A J Jääskeläinen; L Kareinen; T Smura; H Kallio-Kokko; O Vapalahti
Journal:  Infect Ecol Epidemiol       Date:  2020-08-26

3.  Evidence of Chikungunya virus seroprevalence in Myanmar among dengue-suspected patients and healthy volunteers in 2013, 2015, and 2018.

Authors:  Elizabeth Ajema Chebichi Luvai; Aung Kyaw Kyaw; Nundu Sabiti Sabin; Fuxun Yu; Saw Wut Hmone; Kyaw Zin Thant; Shingo Inoue; Kouichi Morita; Mya Myat Ngwe Tun
Journal:  PLoS Negl Trop Dis       Date:  2021-12-01

4.  Estimating chikungunya virus transmission parameters and vector control effectiveness highlights key factors to mitigate arboviral disease outbreaks.

Authors:  Frédéric Jourdain; Henriette de Valk; Harold Noël; Marie-Claire Paty; Grégory L'Ambert; Florian Franke; Damien Mouly; Jean-Claude Desenclos; Benjamin Roche
Journal:  PLoS Negl Trop Dis       Date:  2022-03-04

5.  Aedes albopictus bionomics data collection by citizen participation on Procida Island, a promising Mediterranean site for the assessment of innovative and community-based integrated pest management methods.

Authors:  Beniamino Caputo; Giuliano Langella; Valeria Petrella; Chiara Virgillito; Mattia Manica; Federico Filipponi; Marianna Varone; Pasquale Primo; Arianna Puggioli; Romeo Bellini; Costantino D'Antonio; Luca Iesu; Liliana Tullo; Ciro Rizzo; Annalisa Longobardi; Germano Sollazzo; Maryanna Martina Perrotta; Miriana Fabozzi; Fabiana Palmieri; Giuseppe Saccone; Roberto Rosà; Alessandra Della Torre; Marco Salvemini
Journal:  PLoS Negl Trop Dis       Date:  2021-09-16

6.  Lack of Evidence of Chikungunya Virus Infection among Blood Donors during the Chikungunya Outbreak in Lazio Region, Italy, 2017.

Authors:  Giulietta Venturi; Massimo Fabiani; Antonello Amendola; Giulia Marsili; Eleonora Benedetti; Cristiano Fiorentini; Claudia Fortuna; Simonetta Pupella; Patrizio Pezzotti; Stefania Vaglio; Giulio Pisani; Vincenzo De Angelis; Flavia Riccardo; Ilaria Pati
Journal:  Viruses       Date:  2022-03-16       Impact factor: 5.048

  6 in total

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