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Kassiani Mellou, Georgia Mandilara, Anthi Chrysostomou, Kyriaki Tryfinopoulou, Theologia Sideroglou, Kleon Karadimas, Vasiliki Taxiarhoula Agiassoti, Dimitra Lamprou, Eleni Zampeta, Garyfallia Antoniou, Helen C Maltezou, George Panayiotakopoulos, Public health and clinical implications of multidrug-resistant shigellosis cases in a reception centre for refugees/migrants, Greece, October–December 2019, European Journal of Public Health, Volume 31, Issue 3, June 2021, Pages 588–590, https://doi.org/10.1093/eurpub/ckaa220
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Abstract
From October to December 2019, 18 shigellosis cases (median age: 4.3 years, range: 0–21) were identified in the Reception Center for refugees/migrants on the Greek island of Samos. Fifteen cases (83.3%) were Afghani. Median time from arrival to symptoms onset was 53 days (40–101). Isolates from 14 cases, serotyped as Shigella flexneri 1b, and from three cases, serotyped as S. sonnei phase S (I), presented a multidrug-resistant phenotype. S. flexneri 1b isolates also produced extended-spectrum β-lactamases. Shigella flexneri 2a isolate from the remaining case was resistant to sulfomethoxazole, trimethoprim and pefloxacin. Improvement of hygiene and strengthening of laboratory investigation is needed.
Introduction
Shigella spp. is a member of the Gram-negative Enterobacteriaceae family. It is estimated to cause more than 125 million diarrhoeal episodes annually, leading to around 160 000 deaths.1 Shigellosis spreads by faecal–oral transmission and results in an aggressive watery or mucoid/bloody diarrhoea.1 It is the main bacterial diarrhoeal disease in the childhood population in South Asia and sub-Saharan Africa.2
In the EU/EAA countries, shigellosis is a rare disease with a mean notification rate of 1.98/100 000 in 2018.3 In Greece, shigellosis cases are sporadic or regard small clusters mainly in the population of Roma.4
Since the beginning of 2015, the arrivals of refugees, migrants and asylum seekers to Europe has rapidly increased.5 At countries of entry, most people are first hosted in reception and identification centres (RICs) and are then transferred to more stable hosting facilities (e.g. camps, hostels).6 In 2019, the number of sea arrivals in Greece (59 726) was significantly increased compared to 2018 (32 494) leading to an increased number of hosted people at the five RICs of the North-eastern Aegean Sea.5
The objective of this article is to summarize the available data on the occurrence of multidrug-resistant shigellosis cases in one of the RICs, in Greece, in late 2019, and the consequential public health and clinical implications.
In this article, we refer to refugees, asylum seekers and newly arrived migrants as migrants.
Methods
Setting
The RIC of Samos has a hosting capacity of 648 people.6 During the last trimester of 2019, more than 7000 people were hosted there.5 The majority of them were from Afghanistan (37%) and Syria (28%) and more than half were women (23%) and children (36%).5
Identification of cases and further investigation
The General Hospital of the island reported laboratory-confirmed shigellosis cases in the hosted population of the RIC in early October 2019 via the Mandatory Notification System.
A case investigation form was filled in for each one of the reported cases and the local public health authorities were informed.
We requested cases with diarrhoeas persisting for more than 3 days and fever (≥38 C°) and cases with bloody diarrhoeas to be referred to the hospital for laboratory testing.
A limited number of stool samples were also sent to the Central Public Health Laboratory (CPHL) of National Public Health Organization (NHPO) for testing using the Multiplex PCR method (FilmArray® GI panel) for 22 different pathogens since the local hospital could only test samples for Salmonella spp. and Shigella spp.
Shigella isolates were sent to the National Reference Center for further testing.
Results
From 1 October to 12 December 2019, 18 shigellosis cases were identified. The median age of cases was 4.3 years (range: 0–21 years) and 10 cases (56%) were males. Fifteen cases (83.3%) were from Afghanistan, two from Syria (11.1%) and one from Palestine (5.6%). No cases were identified among the people working/volunteering at the RIC or in the community. The distribution of cases by week of symptoms onset is presented in figure 1. The median time from the arrival at the RIC to the onset of symptoms was 53 days (range: 40–101 days).

Distribution of laboratory confirmed shigellosis cases among refugees/migrants hosted at the reception and identification centre, by week of symptoms onset and serotype, Greece, October–December 2019 (n = 18)
Six samples that were tested positive for Shigella/Enteroinvasive Escherichia coli (EIEC) at the CPHL were also positive for other pathogens (Giardia lamblia, Cryptosporidium parvum, EIEC, etc.).
Shigella spp. isolates were serotyped; 14 as S. flexneri 1b, one as S. flexneri 2a and three as S. sonnei phase S (I).
The S. flexneri 1b isolates presented a multidrug-resistant (MDR) phenotype, according to EUCAST breakpoints; being resistant to third-generation cephalosporins, co-trimoxazole, chloramphenicol, fluoroquinolones (pefloxacin), amoxicillin-clavulanic. Shigella flexneri 1b and S. sonnei phase S (I) isolates exhibited a positive phenotypic test for production of extended-spectrum β-lactamases (ESBLs) and the blaCTX-M-group 1 gene was identified. Regarding azithromycin, all isolates (except for S. flexneri 2a) were considered to belong to the wild population exhibiting inhibition zone diameters higher than the epidemiological cut-off value (ECOFF) (>12 mm). The S. flexneri 2a isolate was resistant to co-trimoxazole, pefloxacin and susceptible to ceftazidime and cefotaxime only in increased exposure; regarding azithromycin, the isolate belonged to non-wild population (inhibition zone diameter = 6 mm).
Two cases of S. flexneri 1b belonged to the same family (siblings). No epidemiological link was identified among the remaining cases apart from being hosted at the same RIC.
Onsite inspection of living conditions concluded sanitation was suboptimal and conducive for infection diseases transmission.
Finally, one additional case of S. sonnei (female, 32 years old, from Iraq), epidemiologically associated with the population of the RIC, was reported from the mainland. The case had been transferred to a camp from the RIC on 22nd of October and presented symptoms on the 23rd. The isolate was not further typed.
No shigellosis cases were reported in the following weeks.
Measures taken
Cases were treated accordingly to the results of the antimicrobial susceptibility testing. Recommendations regarding hygiene measures were given to the population and the personnel of the RIC and the director of the camp. Camps that were going to host population from Samos were informed on the possibility of cases to occur and on the importance of hygiene measures in preventing transmission of shigellosis.
Discussion
Here, we report on the occurrence of multi-drug resistant shigellosis cases among migrants in a RIC on a Greek island between October and December 2019.
Shigellosis cases have been reported among migrants moving through Turkey and Greece, and then via the Balkans to Central Europe.7,8 This is not unexpected according to ECDC given the hygienic conditions during the migration route, as well as in the reception centres; furthermore, high prevalence of shigellosis is recorded in many home countries and countries the migrants travel through.8 This is the second identified increase of shigellosis cases among migrants in Greece after 2015.9
Given the median interval from the arrival at the RIC until the onset of symptoms, cases were infected inside the RIC. The majority of cases were children either due to their poor compliance with hygiene measures or due to the increased seeking of medical attention and testing for children.
Laboratory investigation showed that there were multiple pathogens circulating at the RIC and that the improvement of sanitation conditions was imperative.
The multidrug phenotype of Shigella isolates emphasise the role of antimicrobial susceptibility testing in order cases to receive the appropriate treatment.10 The healthcare personnel should suspect diseases that are not normally seen in the general population, such as shigellosis, and avoid treating patients empirically.
The prevention of further transmission of shigellosis was challenging due to the continuous arrivals at the RIC, overcrowding and the mobility of the population from the islands to the mainland.
Due to the limited resources of the local hospital diagnosis of less severe cases might have been missed. Thus, we cannot define when the first cases occurred. The lack of capacity for analysis of Shigella strains by core genome MLST at the reference centre was another limitation of the investigation.
Overall, the population at RICs should not surpass their hosting capacity and the duration of stay should be as short as possible for the prevention of infectious diseases. Improvement of hygiene conditions and increasing of the laboratory capacity of local hospitals is needed for the prevention, the early identification and the treatment of new cases.
Conflicts of interest: None declared.
Due to the increased influx of migrants/refugees in Europe diseases that are no longer considered public health priorities, such as shigellosis, may re-emerge.
Overcrowding and suboptimal hygiene conditions inside reception and identification centres for newly arrived migrants conduce the transmission of infectious diseases.
Gastroenteritis cases inside camps should be laboratory investigated for the identification of clusters and multi-drug resistant pathogens.
Antimicrobial susceptibility testing for all shigellosis cases is a prerequisite for receiving the appropriate treatment.
References
European Centre for Disease Prevention and Control (ECDC). Surveillance Atlas of Infectious Diseases. Available at: https://atlas.ecdc.europa.eu/public/index.aspx. (3 June
National Public Health Organization (NHPO). Epidemiological data for shigellosis in Greece 2004-2018. Mandatory notification system. National Reference Centre for Salmonella and Shigella. Available at: https://eody.gov.gr/wp-content/uploads/2019/08/Epidemiological-data-for-shigellosis_2004-2018.pdf (3 June 2020, date last accessed).
United Nations High Commissioner for Refugees (UNHCR). Refugees/Migrants Emergency Response–Mediterranean/Greece. Available at: https://data2.unhcr.org/en/situations/mediterranean/location/5179 (1 June 2020, date last accessed).
Asylum Information Database Reception and Identification procedure Greece (AIDA). Available at: https://www.asylumineurope.org/reports/country/greece/asylum-procedure/access-procedure-and-registration/reception-and (2 June 2020, date last accessed).
European Centre for Disease Prevention and Control (ECDC). Rapid Risk Assessment. Shigellosis among refugees in the EU.
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