Travel-associated Legionnaires Research Articles

Incidence of Legionnaires' Disease among Travelers Visiting Hotels in Germany, 2015-2019.

We determined whether the incidence rates of travel-associated Legionnaires' disease (TALD) in hotels in Germany increased after a previous occurrence and whether control measures required by the European Legionnaires' Disease Surveillance Network after a cluster (>2 cases within 2 years) restored the rate to baseline. We analyzed TALD surveillance data from Germany during 2015-2019; a total of 307 TALD cases (163 domestic, 144 nondomestic) in hotels were reported. The incidence rate ratio was 5.5 (95% CI 3.6-7.9) for a second case and 25 (95% CI 11-50) for a third case after a cluster had occurred, suggesting that control measures initiated after the occurrence of TALD clusters might be inadequate to restore the incidence rate to baseline. Our findings indicate that substantial LD preventive measures should be explored by hotels or other accommodations after the first TALD case occurs to reduce the risk for future infections.

Legionella spp. Monitoring in the Water Supply Systems of Accommodation Facilities in Sardinia, Italy: A Two-Year Retrospective Analysis.

Travel-associated Legionnaires' disease is a significant public health concern worldwide. A high number of cases are reported every year among travellers who stay at guest houses, hotels, and spas. Indeed, hot water systems, showers, and air-conditioning systems can be contaminated by Legionella, which grows at 25-42 °C. Studies have shown that in Sardinia, especially during the summer months, the water circulation in the hotels' pipes is exposed to extremely high temperatures. As a result, this study was conducted to assess the colonization of hotel water systems by Legionella in Sardinia, concerning a recent EU directive 2020/2184 for drinking water with a limit of 1000 CFU /L. Methods. A total of 112 accommodation facilities were analyzed, of which 61.3% were found to be colonized with Legionella, and out of a total of 807 samples, 32.5% were positive for Legionella presence. The results showed a higher number of positive samples in the summer season. This was also associated with the higher concentration presence of >1000 CFU/L in the samples. Consequently, this study confirms that local hotel operators should improve their water safety and prevention plans, especially in spring and summer.

Prevalence and Genetic Diversity of Legionella spp. in Hotel Water-Supply Systems in Latvia.

Legionella is one of the most important waterborne pathogens that can lead to both outbreaks and sporadic cases. The majority of travel-associated Legionnaires' disease (TALD) cases are contracted during hotel stays. The aim of this study was to evaluate the prevalence and genetic diversity of Legionella spp. in hotel water supply systems in Latvia. In total, 834 hot water samples were collected from the water systems of 80 hotels in Latvia. At least one Legionella spp. positive sample was detected in 47 out of 80 hotels (58.8%). Overall, 235 out of 834 samples (28.2%) were Legionella spp. positive. The average hot water temperature in Latvian hotels was 49.8 °C. The most predominant L. pneumophila serogroup (SG) was SG3 which was found in 113 (49.8%) positive samples from 27 hotels. For 79 sequenced L. pneumophila isolates, 21 different sequence types (ST) were obtained, including 3 new types-ST2582, ST2579, and ST2580. High Legionella contamination and high genetic diversity were found in the hotel water supply systems in Latvia, which, together with the insufficient hot water temperature, may indicate that the lack of regulation and control measures may promote the proliferation of Legionella.

Javnozdravstveni nadzor nad legionarskom bolešću povezanom sa putovanjima u Evropi i Crnoj Gori

The aim of this study is to show how public health surveillance of travel-associated Legionnaires' disease was conducted in Europe, as well as in Montenegro. The estimations of the European Centre for Disease Prevention and Control (ECDC) indicate that every year about one thousand tourists from Europe get infected by legionellae during their holiday and stay at hotels across the continent. The European Legionnaires' Disease Surveillance Network (ELDSNet) was established with the aim to detect, control and prevent cases, clusters and sources of outbreaks of travel-associated Legionnaires' disease within the European Union (EU) and European Economic Area (EEA), and to assist with detection and response to outbreaks outside the EU/EEA. Sharing information leads to concrete and timely actions of member states of ELDSNet, so that residents of the EU/EEA who travel abroad are protected. ECDC recommends a set of measures that should be followed by public health authorities and tourist sector of the country which was visited by the traveler who caught this disease. If the measures are not carried out, information is published online and European tour operators can use the information when booking holiday packages abroad. Operating procedures provide a set of common measures which should be followed by all EU/ EEA member states involved in the protection of their residents against Legionnaires' disease. Each case of Legionnaires' disease which is reported in tourists, who stayed in Montenegro, is epidemiologically analyzed according to the operating procedures of ELDS Network.

Legionella spp. Colonization in Water Systems of Hotels Linked with Travel-Associated Legionnaires’ Disease

Hotel water systems colonized with Legionella spp. have been the source of travel-associated Legionnaires’ disease, and cases, clusters and outbreaks continue to be reported worldwide each year. A total of 132 hotels linked with travel-associated Legionnaires’ disease, as reported through the European Legionnaires’ Disease Surveillance Network, were inspected and tested for Legionella spp. during 2000–2019 by the public health authorities of the island of Crete (Greece). A total of 3311 samples were collected: 1885 (56.93%) from cold water supply systems, 1387 (41.89%) from hot water supply systems, 37 (1.12%) were swab samples and two (0.06%) were soil. Of those, 685 (20.69%), were collected from 83 (62.89%) hotels, testing positive (≥50 CFU/L) for Legionella pneumophila) serogroups 1–10, 12–14 and non-pneumophila species (L. anisa, L. erythra, L. tusconensis, L. taurinensis, L. birminghamensis, L. rubrilucens, L. londiniesis, L. oakridgensis, L. santicrusis, L. brunensis, L. maceacherii). The most frequently isolated L. pneumophila serogroups were 1 (27.92%) and 3 (17.08%). Significantly higher isolation rates were obtained from hot water supply systems (25.96%) versus cold water systems (16.98%) and swab samples (13.51%). A Relative Risk (R.R.) > 1 (p < 0.0001) was calculated for hot water temperature <55 °C (R.R.: 4.43), chlorine concentrations <0.2 mg/L (R.R.: 2.69), star ratings <4 (R.R.: 1.73) and absence of Water Safety Plan implementation (R.R.: 1.57).

European Surveillance of Legionnaires' Disease.

Legionnaires' disease and Pontiac fever are both diseases with important public health implications and require prompt and thorough responses to outbreaks for future prevention. Effective methods for defining, diagnosing, reporting and responding to legionellosis outbreaks ideally should be standardized across countries. Therefore, the European Union surveillance methods for countering Legionnaires' disease is a useful model especially for travel-associated Legionnaires' disease (TALD) cases which are on the rise. Multi-country surveillance in the EU and European Economic Area (EEA) has evolved since the first organizational efforts in the 1980's to the currently responsible, European Legionnaires' Disease Surveillance Network (ELDSNet). This chapter outlines the practices of the EU surveillance of Legionnaires' disease including their schemata, definitions, responsibilities of participating members, methods and the results of the data collected since the program's inception. Lastly, improvements must still be made as the incidence of Legionnaires' disease in the EU is likely underestimated due to underreporting and/or underdiagnosis. Nearly 70% of cases are reported from only four countries, France, Germany, Italy and Spain, which represent 50% of the EU population.

Factors associated with Legionnaires' disease recurrence in hotel and holiday rental accommodation sites.

BackgroundThe detection of a cluster of travel-associated Legionnaires’ disease (TALD) cases in any European Union/European Economic Area (EU/EEA) country prompts action at the accommodation, follow-up by health authorities and reporting of measures taken. Some accommodations incur further cases despite presumed implementation of adequate control measures.AimTo identify factors associated with the occurrence of a further TALD case after the implementation of control measures.MethodsWe conducted a retrospective cohort study of hotel and holiday rental accommodations in the EU/EEA associated with two or more TALD cases with onset dates less than 2 years apart (a ‘cluster’) and notification between 1 June 2011−31 December 2016. We fitted Cox regression models to estimate the association between accommodation characteristics and the occurrence of a further case, defined as any case with onset date after the report on measures taken.ResultsOf the 357 accommodations in the analysis, 90 (25%) were associated with at least one further case after the report on measures taken (12.4/100 accommodation-years). Accommodations associated with two or more cases before the cluster notification were more likely to be associated with a further case, compared with those not previously associated with any case (adjusted hazard ratio 1.85; 95% confidence interval: 1.14–3.02). Neither the detection of Legionella in the water system nor the type of disinfection were found to be associated with the risk of a further case.ConclusionAccommodation size and previous TALD cases were predictive of further Legionnaires’ disease cases after implementation of control measures.

Travel-associated Legionnaires' disease: would changing cluster definition lead to the prevention of a larger number of cases?

According to European Guidelines for Legionnaires' Disease prevention and control, travel-associated Legionnaires' disease (TALD) cases are managed differently if classified as sporadic or as part of a cluster and more stringent control measures are deployed after clusters are identified. In this study, we propose to modify the current cluster definition: 'two or more cases of Legionnaires' disease (LD) who stayed at, or visited, the same commercial accommodation site 2-10 days before onset of illness and whose onset is within the same 2-year period' with a new cluster definition, i.e. accommodation sites associated with multiple cases regardless of the time elapsed between them. TALD cases occurred in Italy and in the Balearic Islands between 2005 and 2015 were analysed applying the current European Legionnaires' Disease Surveillance Network (ELDSNet) cluster definition. In a sample of selected accommodation sites with multiple cases, a microbiological study was also conducted. Using the new definition, 63 additional sites (16.4% increase) and 225 additional linked cases (19.5% increase) were identified. Legionella pneumophila sg1 was isolated from 90.7% of the selected accommodation sites. The use of the here proposed TALD cluster definition would warrant a full investigation for each new identified case. This approach should therefore increase the number of sites that will require a risk assessment and, in the presence of an increased risk, the adoption of LD control measures to hopefully prevent additional cases.

Clusters of Legionnaires' disease in period hotels with complex water systems: lessons learnt in the West Midlands, UK

BackgroundIn 2017 there were two distinct clusters of local travel-associated Legionnaires' disease associated with period hotels built in the 17th and 18th centuries in the West Midlands, UK. Both hotels had undergone frequent structural modifications. Five cases occurred 3 months to 2 years apart. The aim of this report is to share the learning from the investigations and challenges faced in achieving control of Legionella pneumophila in the water systems of dated buildings. MethodsEpidemiological information was obtained through structured cases interviews and through linked cases by the national surveillance scheme database. Hotel water system maintenance records were reviewed, and samples were taken at numerous timepoints and different locations, with an initial focus on facilities and rooms used by the cases. Sputum and environmental samples were tested in the reference laboratory and sequence-based typing was undertaken. FindingsUnsatisfactory levels of L pneumophila serogroup 1 were detected from hot and cold water outlets in both hotels. At one of the hotels L pneumophila serogroup 1, sequence type ST62 subtypes in clinical and environmental samples were indistinguishable. Both hotels were closed for business for months to undertake extensive remediation work. This closure was temporarily effective in achieving adequate control of legionella but 6 months later routine monitoring detected unsatisfactory levels. Achieving sustained legionella control in dated water systems and verifying safe endpoints for hotel re-opening has proven challenging for the regulatory bodies. InterpretationSustaining legionella control in the dated water systems of period buildings was demanding, and public confidence in the effectiveness of control measures was compromised. There were four key challenges: defining a cluster and the timely confirmation of when an outbreak has developed; using the cluster and outbreak definitions to inform the risk assessments and review of control measures in the environmental investigations; communicating the risk to the public and the media through clear messages; and seeking assurance on safety of water management systems in defining the endpoint for a cluster or outbreak investigation. FundingNone.

Legionella spp. Risk Assessment in Recreational and Garden Areas of Hotels.

Several Travel-associated Legionnaires’ disease (TALD) cases occur annually in Europe. Except from the most obvious sites (cooling towers and hot water systems), infections can also be associated with recreational, water feature, and garden areas of hotels. This argument is of great interest to better comprehend the colonization and to calculate the risk to human health of these sites. From July 2000–November 2017, the public health authorities of the Island of Crete (Greece) inspected 119 hotels associated with TALD, as reported through the European Legionnaires’ Disease Surveillance Network. Five hundred and eighteen samples were collected from decorative fountain ponds, showers near pools and spas, swimming pools, spa pools, garden sprinklers, drip irrigation systems (reclaimed water) and soil. Of those, 67 (12.93%), originating from 43 (35.83%) hotels, tested positive for Legionella (Legionella pneumophila serogroups 1, 2, 3, 6, 7, 8, 13, 14, 15 and non-pneumophila species (L. anisa, L. erythra, L. taurinensis, L. birminghamensis, L. rubrilucens). A Relative Risk (R.R.) > 1 (p < 0.0001) was calculated for chlorine concentrations of less than 0.2 mg/L (R.R.: 54.78), star classification (<4) (R.R.: 4.75) and absence of Water Safety Plan implementation (R.R.: 3.96). High risk (≥104 CFU/L) was estimated for pool showers (16.42%), garden sprinklers (7.46%) and pool water (5.97%).

Legionnaires' Disease in Hotels and Passenger Ships: A Systematic Review of Evidence, Sources, and Contributing Factors.

Travel-associated Legionnaires' disease (LD) is a serious problem, and hundreds of cases are reported every year among travelers who stayed at hotels, despite the efforts of international and governmental authorities and hotel operators to prevent additional cases. A systematic review of travel-associated LD events (cases, clusters, outbreaks) and of environmental studies of Legionella contamination in accommodation sites was conducted. Two databases were searched (PubMed and EMBASE). Data were extracted from 50 peer-reviewed articles that provided microbiological and epidemiological evidence for linking the accommodation sites with LD. The strength of evidence was classified as strong, possible, and probable. Three of the 21 hotel-associated events identified and four of nine ship-associated events occurred repeatedly on the same site. Of 197 hotel-associated cases, 158 (80.2%) were linked to hotel cooling towers and/or potable water systems. Ship-associated cases were most commonly linked to hot tubs (59/83, 71.1%). Common contributing factors included inadequate disinfection, maintenance, and monitoring; water stagnation; poor temperature control; and poor ventilation. Across all 30 events, Legionella concentrations in suspected water sources were >10,000 cfu/L, <10,000 cfu/L, and unknown in 11, 3, and 13 events, respectively. In five events, Legionella was not detected only after repeated disinfections. In environmental studies, Legionella was detected in 81.1% of ferries (23/28) and 48.9% of hotels (587/1,200), while all 12 cruise ships examined were negative. This review highlights the need for LD awareness strategies targeting operators of accommodation sites. Increased standardization of LD investigation and reporting, and more rigorous follow-up of LD events, would help generate stronger, more comparable evidence on LD sources, contributing factors, and control measure effectiveness.

Colonization of Legionella species in Turkish baths in hotels in Alanya, Turkey.

This study evaluated the prevalence of Legionella species in water samples collected from Turkish baths in hotels in Alanya, Turkey, from August 2003 to September 2013. Water samples were collected in 100-mL sterile containers and then concentrated by filtration. Heat treatment was used to eliminate other microorganisms from the samples, which were then spread on Legionella-selective-buffered charcoal yeast extract alpha (BCYE-α) agar and on BCYE-α agar supplemented with glycine, vancomycin, polymyxin, and cycloheximide. Cysteine-dependent colonies were identified by latex agglutination. In total, 135 samples from 52 hotels with Turkish baths were evaluated. Legionella species were identified in 11/52 (21.2%) hotels and 18/135 (13.3%) samples. The most frequently isolated species was Legionella pneumophila, with most isolates belonging to serogroups 6 (55.6%) and 1 (22.2%). The colony count was <100 colony-forming units (CFU) mL(-1) in nine samples, from 100 to 1000 CFU mL(-1) in six samples, and >1000 CFU mL(-1) in three samples. These findings suggest that the hot water systems of Turkish baths in hotels must be viewed as a possible source of travel-associated Legionnaires' disease, and preventative measures should be put in place.

Travel-associated Legionnaires’ disease in European visitors to South Africa

Travel-associated Legionnaires’ disease in European visitors to South Africa

Travel-associated Legionnaires’ disease in Europe, 2010

In 2010, the European surveillance network for travel-associated Legionnaires' disease (ELDSNet, previously EWGLINET) received reports of 864 cases of travel-associated Legionnaires' disease, of whom 24 were reported to have had a fatal outcome. As in previous years, a very low proportion of clinical isolates were obtained (45 cases, 5.6%). In the 2010 dataset, male cases outnumbered female cases by 2.6:1 and had a median age of 61 years (range: 21-96), while the median age for women was 63 years (range: 12-95). The network identified 100 new clusters in 2010, of which 44 involved only one case from each reporting country and would probably not have been detected by national surveillance schemes alone. The largest cluster (having 14 cases) was associated with a cruise ship. Legionella species were detected at 61 of the 100 accommodation site clusters investigated. The names of five accommodation sites were published on the ECDC website.

Evaluation of a Legionella Outbreak Emerged in a Recently Opening Hotel

Legionnaires' disease (LD) is a systemic infection caused by Legionella species especially colonized in the water systems. Hotels are common locations in which waterwork-associated sporadic or epidemic legionellosis can be detected. The aim of this study was to evaluate a small Legionella outbreak emerged in a recently opened 600-bed hotel in Alanya, a touristic county in Mediterranean part of Turkey. A 66 years old male patient who stayed in this hotel opened on May 15th, 2009, was admitted to our hospital on May 21st, 2009 with the complaints of high fever, headache and diarrhea lasting for three days. Since chest X-ray revealed non-homogenous density increase in left middle and inferior zone, the patient was diagnosed as atypical pneumoniae and LD was confirmed by positive urinary Legionella antigen test (Card test, BinaxNOW®Legionella Urinary Antigen Test; Alere Co, USA) result. Following the identification of the index case, the records of our hospital were reviewed and revealed another case being treated with the diagnosis of community acquired pneumonia who was also the guest of the same hotel. This patient was then diagnosed as LD by positive urinary antigen test. Since new cases were identified during the following days (May 22, 25 and 26) the Antalya County Health Department and hotel management were informed about a cluster of LD. In addition subsequent investigation for environmental surveillance and water sampling were conducted. The LD diagnosis and environmental inspections were performed according to the procedure described in the guideline from "Turkish Ministry of Health Travel-Associated Legionnaires' Disease Control Programme". Five definitive cases and one presumptive case of LD were identified during the outbreak period (May 20-26, 2009). All of the cases were successfully treated (intravenous ciprofloxacin or levofloxacin or clarithromycin), however one patient died due to sudden death during sleep after being discharged. Since sputum samples could not be obtained from the cases, the diagnosis were not confirmed by culture but by urinary antigen test. Besides high antibody titer in single serum sample was accepted as a diagnostic marker. Additionally 26 cases who accommodated in the same hotel and presented with high fever without pneumonia were treated in the outpatient clinics of our hospital. Urinary antigen test was performed in 11 of those patients to confirm the prediagnosis of pontiac fever, however all were found negative. Likewise convalescent phase sera for the confirmation of the diagnosis by seroconversion could not be obtained since they all were foreign tourists. Investigation of water sources of the hotel revealed that the municipal drinking water network had not been connected yet and the hotel supplied water from groundwater sources. The analysis of multiple samples from multiple sites of hotel's water system indicated that the water temperature was between 35-45°C and the iron level was beyond the acceptable limits (245 µg/L) recommended for drinking water in the regulation guides. These properties were considered as the factors that enhanced the growth and survival of Legionella species. Water samples were cultivated on BCYE-_ (Buffered Charcoal Yeast Extract a-Ketoglutarate) and GVPC (Glycine-Vancomycin-Polymyxin-Cycloheximide) agar plates and 11 out of a total 13 samples yielded Legionella spp. growth. All isolates were identified as L.pneumophila serogroup 1 by specific antisera. Legionella decontamination of hotel's water system was managed by implementation of hyperchlorination method as well as superheating (> 60°C) of water. The hotel was not closed during the outbreak and cultures of water samples obtained for one year later did not yield any Legionella spp. growth. This outbreak emphasized that hotel residents are at risk for acquiring LD in the presence of a colonized water system, even in a newly constructed building. In conclusion, effective control and decontamination programmes for the prevention of Legionella colonization should be applied even in new opening hotels.

Risk for Travel-associated Legionnaires’ Disease, Europe, 2009

Legionnaires' disease is underreported in Europe; notification rates differ substantially among countries. Approximately 20% of reported cases are travel-associated. To assess the risk for travel-associated Legionnaires' disease (TALD) associated with travel patterns in European countries, we retrieved TALD surveillance data for 2009 from the European Surveillance System, and tourism denominator data from the Statistical Office of the European Union. Risk (number cases reported/number nights spent) was calculated by travel country. In 2009, the network reported 607 cases among European travelers, possibly associated with 825 accommodation sites in European Union countries. The overall risk associated with travel abroad was 0.3 cases/million nights. We observed an increasing trend in risk from northwestern to southeastern Europe; Greece had the highest risk (1.7). Our findings underscore the need for countries with high TALD risks to improve prevention and control of legionellosis; and for countries with high TALD risks, but low notification rates of Legionnaires' disease to improve diagnostics and reporting.

Travel-associated Legionnaires’ disease in residents from England and Wales travelling to Corfu, Greece, August to October 2011

Fourteen cases of Legionnaires’ disease were confirmed in residents from England and Wales with history of travel to Corfu, Greece, in the 14 days before symptom onset. These cases were reported to the Health Protection Agency national surveillance scheme for Legionnaires’ disease in residents of England and Wales between August and October 2011. In addition, one case in a Greek national and a case of non-pneumonic legionellosis in a resident from Scotland were also reported. Few cases shared the same accommodation site in Corfu during their incubation period. Epidemiological investigations and microbiological analysis of clinical and environmental samples excluded a single source but rather implicated several accommodation sites as sources of sporadic infection. Control measures have since been implemented at these accommodation sites and no further cases have been reported. This incident highlights the value of epidemiological typing and the importance of effective international response to control and prevent legionella infection.

Cluster of travel-associated Legionnaires’ disease in Lazise, Italy, July to August 2011

Since 18 August 2011, 17 cases of travel-associated Legionnaires' disease have been reported. They were tourists from five European countries who had stayed in five accommodation sites in Lazise, Italy. The dates of symptom onset ranged from 18 July to 25 August 2011. Control measures were implemented and no further cases associated with stays at the sites have been reported after disinfection. Timely notification of any further cases potentially associated with stay in Lazise is recommended.

Travel-associated Legionnaires disease: clinical features of 17 cases and a review of the literature

We retrospectively investigated patients with Legionnaires disease (LD) who had been admitted to the Baskent University Alanya Teaching and Research Hospital, Ankara, Turkey, from January 2002 to September 2009. Twenty definitive cases were followed as LD, 17 (85%) of which were travel associated. The mean age was 61.5 ± 9.5 years (range, 39–77 years). Diabetes mellitus was found in 7 (41.2%) of those patients. Gastrointestinal or neurologic abnormalities were found approximately in two-thirds and relative bradycardia in 9 (52.9%). LD was severe in 11 (64.7%) patients, which required intensive care unit follow-up. Although appropriate antibiotic therapy was initiated in all patients on admission day, 4 (23.5%) deaths occurred. In conclusion, clinicians should remain vigilant about the diagnosis of LD in patients with community-acquired pneumonia, especially in the presence of extrapulmonary involvement, risk factors for LD, and a history of recent travel. As in our cases, mortality is still high in sporadic cases despite early appropriate treatment.

Travel-associated Legionnaires’ disease in Europe in 2009

A total of 818 cases of Legionnaires' disease with onset of illness in 2009 were reported from 22 European and two non-European countries to the European Surveillance Scheme for Travel-Associated Legionnaires' Disease (EWGLINET). This is a decrease of 52 cases compared with 2008 and 129 fewer than in 2007 - the peak year of reporting to date. A total of 794 (97.1%) cases were reported as confirmed and 24 as presumptive cases. Outcome of illness was reported for 561 (68.6%) cases. Of these cases 28 (5%) were reported to have died. More than half, of the cases in 2009 (n=469, 57.3%) were reported within 20 days of symptom onset. Cases visited 53 countries and were infected in all months of the year, with a peak in September (n=146). By country of residence of the cases, the United Kingdom (UK) reported the highest number of cases (n=173). Italy reported the second highest number of cases (n=169) and was also the country associated with the most cases by country of infection (n=209). A total of 88 new clusters (75 in Europe and 13 outside Europe) were detected in 2009 and were associated with 196 cases. The largest cluster occurred in Italy and involved seven cases. Without the scheme's international database, thirty three (37.5%) of the newly detected clusters would not have been identified. In 49 of the accommodation sites with clusters of cases, environmental samples were found to be positive for Legionella spp. Details of 10 sites were published on the European Working Group for Legionella Infections (EWGLI) website for failure to return information on the status of environmental investigations.