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A small sample of Legionella literature.

Legionella literature

 

Legionella Colonization of Hotel Water Systems in Touristic Places of Greece: Association with System Characteristics and Physicochemical Parameters. / Kyritsi MA, Mouchtouri VA, Katsioulis A, Kostara E, Nakoulas V, Hatzinikou M, Hadjichristodoulou C. / Int J Environ Res Public Health. 2018 Nov 30;15(12). pii: E2707. doi: 10.3390/ijerph15122707. / https://www.ncbi.nlm.nih.gov/pubmed/30513698

This study aimed to assess the colonization of hotel water systems in central Greece and Corfu by Legionella, and to investigate the association between physicochemical parameters and Legionella colonization. Standardized hygiene inspection was conducted in 51 hotels, and 556 water samples were analyzed for Legionella spp. Free chlorine concentration, pH, hardness, conductivity, and trace metals were defined in cold water samples. The results of inspections and chemical analyses were associated with the microbiological results using univariate and logistic regression analysis. According to the score of the checklist used for the inspections, 17.6% of the hotels were classified as satisfactory, 15.7% as adequate, and 66.7% as unsatisfactory. Moreover, 74.5% of the hotels were colonized by Legionella spp. and 31.4% required remedial measures according to the European guidelines. Legionella spp. were isolated in 28% of the samples. Unsatisfactory results of inspections were associated with Legionella presence (relative risk (RR) = 7.67, p-value = 0.043). In hot-water systems, <50 °C temperatures increased the risk of Legionella colonization (RR = 5.36, p-value < 0.001). In cold-water systems, free chlorine concentration <0.375 mg/L (odds ratio (OR) = 9.76, p-value = 0.001), pH ≥ 7.45 (OR = 4.05, p-value = 0.007), and hardness ≥321 mgCaCO₃/L (OR = 5.63, p-value = 0.003) increased the risk, whereas copper pipes demonstrated a protective role (OR = 0.29, p-value = 0.0024). The majority of the hotels inspected were colonized with Legionella. Supplementary monitoring of the risk factors that were identified should be considered.

Effectiveness of a neutral electrolysed oxidising water (NEOW) device in reducing Legionella pneumophila in a water distribution system: A comparison between culture, qPCR and PMA-qPCR detection methods. / Bonetta S, Pignata C, Bonetta S, Meucci L, Giacosa D, Marino E, Gorrasi I, Gilli G, Carraro E. / Chemosphere. 2018 Nov;210:550-556. doi: 10.1016/j.chemosphere.2018.07.053. Epub 2018 Jul 11. / https://www.ncbi.nlm.nih.gov/pubmed/30029147

Disinfection of hot water systems is critical for reducing Legionnaires' disease inhigh-risk buildings. The use of neutral electrolysed oxidising water (NEOW) is a promising method for the control of microorganisms in hot water systems. However, full-scale evaluations of the efficacy of NEOW devices to control Legionella pneumophila are currently lacking. The aim of this study was to assess the effectiveness of a NEOW device in reducing L. pneumophila in a hotel water network. Water samples (n = 67) were collected from different sites of a hotel distribution system before and after the installation of the NEOW device at the 1st, 4th, 8th and 12th week. Detection of L. pneumophila was performed comparing culture, qPCR and PMA-qPCR methods. Total bacterial counts (22 °C and 37 °C), Pseudomonas spp. and physico-chemical parameters were also monitored. The NEOW treatment resulted in a reduction of the amount of L. pneumophila positive samples (-32%) and of the number of heavily contaminated points (>104 CFU/L and >103 CFU/L) (-100% and -96%, respectively). Treatment maintained L. pneumophila at low levels (<102 CFU/L), which do not require specific intervention measures. The effectiveness of the disinfection system was also confirmed by PMA-qPCR (p < 0.001). The use of PMA resulted in a signal decrease in almost all samples upon the disinfection treatment. The NEOW disinfection device appears to be a promising approach to reduce the colonisation of hot water systems by L. pneumophila; however, further investigations are needed to ascertain its efficiency over longer time periods.

Shiga toxin-producing Escherichia coli O103:H2 outbreak in Germany after school trip to Austria due to raw cow milk, 2017 - The important role of international collaboration for outbreak investigations. / Mylius M, Dreesman J, Pulz M, Pallasch G, Beyrer K, Claußen K, Allerberger F, Fruth A, Lang C, Prager R, Flieger A, Schlager S, Kalhöfer D, Mertens E. / Int J Med Microbiol. 2018 Jul;308(5):539-544. doi: 10.1016/j.ijmm.2018.05.005. Epub 2018 May 29. / https://www.ncbi.nlm.nih.gov/pubmed/29884330

Following a school ski-trip to Austria from 10 to 18/02/2017, nine of 25 participants of the group from Lower Saxony (Germany) developed gastroenteritis. The students and teachers (17-41 years) shared meals in a hotel. Active case finding revealed further cases among German school groups from North Rhine-Westphalia and Schleswig-Holstein, staying at the same hotel in February 2017. We conducted two retrospective cohort studies using self-administered questionnaires on clinical symptoms and food consumption. We defined a case as a trip participant in February 2017, staying at the aforementioned hotel and developing diarrhoea, vomiting or abdominal pain during or within ten days after the trip and/or who had a stool sample tested positive for STEC within four weeks after the trip. During the outbreak investigation, Austrian authorities detected that unlabeled raw cow milk delivered by a dairy farm had been offered at the hotel for breakfast during January and February 2017. Stool samples of participants, samples of milk served in the hotel and fecal samples of various animals kept at the milk-delivering farm were examined by culture and polymerase chain reaction. STEC isolates were typed using Pulsed-field Gel Electrophoresis (PFGE) and Whole-Genome Sequencing (WGS). All 25 participants from Lower Saxony completed the questionnaire on symptoms and milk consumption; 14 were cases (56%). Thirteen of 20 participants who had consumed cold milk fell ill (risk ratio (RR): 3.25; 95%-confidence interval (CI): 0.55-19.32). Of 159 trip participants from North Rhine-Westphalia, 81 completed the questionnaire (51%), 25 were cases (31%); RR for cold milk was 2.11 (CI: 0.89-5.03). The combined RR for cold milk in both groups was 2.49 (CI: 1.16-5.35). Shiga toxin 1a-gene and eaeA-gene positive STEC O103:H2 were detected in nine of 32 patients' stool samples and in two of 18 dairy farm cattle. Nine isolates from human stool samples and two isolates from cattle fecal samples yielded the same strain with an almost identical PFGE-pattern and WGS-profile. Microbiological and epidemiological evidence identified raw cow milk as the vehicle. Results may have been compromised by misclassification of cases due to a recall bias and mild symptoms. As a result of this outbreak investigation, the Austrian authorities enforced Austrian law in the hotel, to provide milk only when pasteurized. We recommend re-emphasizing the risk of raw milk consumption to providers.

Legionella spp. Risk Assessment in Recreational and Garden Areas of Hotels. / Papadakis A, Chochlakis D, Sandalakis V, Keramarou M, Tselentis Y, Psaroulaki A. / Int J Environ Res Public Health. 2018 Mar 26;15(4). pii: E598. doi: 10.3390/ijerph15040598. / https://www.ncbi.nlm.nih.gov/pubmed/29587446

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%).

Notes from the Field: Legionellosis Outbreak Associated with a Hotel Aquatics Facility - Tennessee, 2017. / Yackley JK, Sweat D, Fill MA, Garman K, Dunn JR. / MMWR Morb Mortal Wkly Rep. 2018 Jan 19;67(2):77-78. doi: 10.15585/mmwr.mm6702a5. No abstract available. / https://www.ncbi.nlm.nih.gov/pubmed/29346335

On June 26, 2017, the Tennessee Department of Health (TDH) was notified by CDC of two travel-associated cases of legionellosis. The patients resided in Florida and the United Kingdom but had a common hotel exposure in Memphis, Tennessee. On June 27, the Shelby County Health Department identified a third case in a Shelby County resident with the same hotel exposure. All three persons had positive Legionella urinary antigen tests and reported using the hotel hot tub. A joint state and local investigation was launched, which included environmental health, epidemiologic, and laboratory components. Shelby County environmental health specialists conducted an assessment of the hotel aquatics facility and identified improper water treatment monitoring and low chlorine residuals (0 ppm; acceptable range = 1–3 ppm). On June 28, TDH was notified of four additional travel companions with illness after exposure to the hotel aquatics facility, including two persons with confirmed Legionella, one of whom died.

Rare presentation of an old bug. / Albitar HAH, Gallo de Moraes A, Lim KG. / BMJ Case Rep. 2017 Oct 19;2017. pii: bcr-2017-220959. doi: 10.1136/bcr-2017-220959. / https://www.ncbi.nlm.nih.gov/pubmed/29054940

We highlight a rare presentation of Legionella infection in a 77-year-old woman with a clinical diagnosis of giant cell arteritis 2 months prior to presentation. She was started on 60 mg prednisone that was tapered to 10 mg after 4 weeks following her diagnosis. She presented with a 1-month progressive dyspnoea in the absence of any other symptoms. Her exposure history was significant only for a recent trip to Florida where she stayed at a hotel. Initial laboratory workup was significant for hyponatraemia (127 mmol/L). Workup including bronchoalveolar lavage (BAL) and induced sputum for gram stain, acid fast stain and bacterial culture were negative for Pneumocystis jirovecii pneumonia and other opportunistic infectious agents. However, BAL was positive for Legionella pneumophila via PCR that was confirmed by a positive urinary Legionella antigen. The patient received treatment with levofloxacin that led to full resolution of her symptoms.

Legionellosis: a Walk-through to Identification of the Source of Infection. / Chochlakis D, Sandalakis V, Keramarou M, Tselentis Y, Psaroulaki A. / Cent Eur J Public Health. 2017 Sep;25(3):235-239. doi: 10.21101/cejph.a4660. / https://www.ncbi.nlm.nih.gov/pubmed/29022684

Although a number of human Legionnaires' disease in tourists are recorded annually in Europe, there are few cases where a direct link can be made between the infected person and the source of infection (hotel or other accommodation). We present a scheme followed in order to track down and identify the source of infection in a tourist suffering from L. pneumophila sg 5 infection, who was accommodated in seven different hotels during his holidays in the island of Crete, and we comment on various difficulties and draw-backs of the process. Water samples were collected from the seven hotels where the patient had resided and analyzed at the regional public health laboratory using cultivation and molecular tests. Of 103 water samples analyzed, 19 (18.4%) were positive for Legionella non-pneumophila and 8 (7.8%) were positive for L. pneumophila. A successful L. pneumophila sg 5 match was found between the clinical and environmental sample, which led us to the final identification of the liable hotel. Timely notification of the case, within the the European Legionnaires' Disease Surveillance Network (ELDSNet) of the partners involved, is crucial during a course of travel associated with Legionella case investigation. Moreover, the urinary antigen test alone cannot provide sufficient information for the source identification. However, acquiring clinical as well as environmental isolates for serogroup and SBT identification is highly important for the successful matching.

Exploring the Legionella pneumophila positivity rate in hotel water samples from Antalya, Turkey. / Sepin Özen N, Tuğlu Ataman Ş, Emek M. / Environ Sci Pollut Res Int. 2017 May;24(13):12238-12242. doi: 10.1007/s11356-017-8864-1. Epub 2017 Mar 29. / https://www.ncbi.nlm.nih.gov/pubmed/28353109

The genus Legionella is a fastidious Gram-negative bacteria widely distributed in natural waters and man made water supply systems. Legionella pneumophila is the aetiological agent of approximately 90% of reported Legionellosis cases, and serogroup 1 is the most frequent cause of infections. Legionnaires' disease is often associated with travel and continues to be a public health concern at present. The correct water management quality practices and rapid methods for analyzing Legionella species in environmental water is a key point for the prevention of Legionnaires' disease outbreaks. This study aimed to evaluate the positivity rates and serotyping of Legionella species from water samples in the region of Antalya, Turkey, which is an important tourism center. During January-December 2010, a total of 1403 samples of water that were collected from various hotels (n = 56) located in Antalya were investigated for Legionella pneumophila. All samples were screened for L. pneumophila by culture method according to "ISO 11731-2" criteria. The culture positive Legionella strains were serologically identified by latex agglutination test. A total of 142 Legionella pneumophila isolates were recovered from 21 (37.5%) of 56 hotels. The total frequency of L. pneumophila isolation from water samples was found as 10.1%. Serological typing of 142 Legionella isolates by latex agglutination test revealed that strains belonging to L. pneumophila serogroups 2-14 predominated in the examined samples (85%), while strains of L. pneumophila serogroup 1 were less numerous (15%). According to our knowledge, our study with the greatest number of water samples from Turkey demonstrates that L. pneumophila serogroups 2-14 is the most common isolate. Rapid isolation of L. pneumophila from environmental water samples is essential for the investigation of travel related outbreaks and the possible resources. Further studies are needed to have epidemiological data and to determine the types of L. pneumophila isolates from Turkey.

Microbiology and Epidemiology of Legionnaire's Disease. / Burillo A, Pedro-Botet ML, Bouza E. / Infect Dis Clin North Am. 2017 Mar;31(1):7-27. doi: 10.1016/j.idc.2016.10.002. Review. / https://www.ncbi.nlm.nih.gov/pubmed/28159177

Legionnaire's disease (LD) is the pneumonic form of legionellosis caused by aerobic gram-negative bacilli of the genus Legionella. Individuals become infected when they inhale aerosolized water droplets contaminated with Legionella species. Forty years after the identification of Legionella pneumophila as the cause of the 1976 pneumonia outbreak in a hotel in Philadelphia, we have non-culture-based diagnostic tests, effective antibiotics, and preventive measures to handle LD. With a mortality rate still around 10%, underreporting, and sporadic outbreaks, there is still much work to be done. In this article, the authors review the microbiology, laboratory diagnosis, and epidemiology of LD.

Travel-associated infections caused by unusual serogroups of Legionella pneumophila identified using Legionella BIOCHIP slides in Turkey and Iraq. / Kocazeybek BS, Yuksel P, Keskin D, Sheikh S, Habip Z, Yavuzer SS, Caliskan R, Altun YM, Kuskucu M, Cengiz M, Dinc HO, Karakullukcu A, Ergin S, Saribas S, Yilmaz N, Tokman HB. / Travel Med Infect Dis. 2016 May-Jun;14(3):248-54. doi: 10.1016/j.tmaid.2016.04.001. Epub 2016 Apr 19. / https://www.ncbi.nlm.nih.gov/pubmed/27108684

Although Legionella pneumophila serogroup 1 is the common disease causing serogroup, rare serogroups can also may cause legionellosis. A 54-year-old male patient (index case) reported that he had been on a religious trip (for visiting, tomb of Ali, which is important for Shias) to Iraq with a large group (50 shia pilgrims from Kars city of Turkey) two weeks prior to admission. Due to civil war, the hotel where the patient stayed in Iraq lacked proper hygiene. A large number of people in the travel group were experiencing the same symptoms. Other five cases were 2 males (ages; 50, 45) and 3 females including the wife of the index case (ages; 50, 28, 27). The detection of L. pneumophila IgG and IgM was performed by anti-L. pneumophila Indirect Immunofluorescent IgM, IgG kit. Legionella 1 biochip/verification BIOCHIP slides were used for serogrouping in Euroimmun AG, Leubeck, Germany. In index case, L. pneumophila IgM was positive with a titer of 1/32 titer. IgG was negative with a 1/100 titer. Another case (28 year old female), had clinical symptoms identical to the index case. L. pneumophila IgM and IgG were positive with titers of 1/64 and 1/100, respectively. These two cases were diagnosed with Legionnaires' disease caused by L. pneumophila serogroup 12 (index case) and female (28-year-old) by serogroup 11. The other 4 cases were diagnosed with possible Pontiac fever caused by L. pneumophila serogroups 14 (wife of the index case), 4, and 6 whereas the serogroup of L. pneumophila detected in 27 years old female case could not be identified. A major limitation of this work is the absence of genotyping and the serogroup difference between index case and his wife who shared the same hotel. We suggest that this serogroup difference may be caused by (for men and women) sitting separately in Islamic rules. On the other hand, the movement of people in the context of mutual visits between countries or neighboring countries for tourism-related (i.e., for religious events or visits to holy sites) or immigration-related reasons, may cause some epidemic diseases. This study reemphasized that not only L. pneumophila serogroup 1, but other rare serogroups might cause also legionellosis which may increase in frequency and cause regional epidemics. We propose that increased financial resources for improving the hygiene conditions and performing routine legionella surveillance studies in touristic hotels would be useful measures for legionellosis prevention and control.

Genomic Investigation of a Legionellosis Outbreak in a Persistently Colonized Hotel. / Sánchez-Busó L, Guiral S, Crespi S, Moya V, Camaró ML, Olmos MP, Adrián F, Morera V, González-Morán F, Vanaclocha H, González-Candelas F. / Front Microbiol. 2016 Jan 21;6:1556. doi: 10.3389/fmicb.2015.01556. eCollection 2015. / https://www.ncbi.nlm.nih.gov/pubmed/26834713

Legionellosis Outbreak Associated With a Hotel Fountain. / Smith SS, Ritger K, Samala U, Black SR, Okodua M, Miller L, Kozak-Muiznieks NA, Hicks LA, Steinheimer C, Ewaidah S, Presser L, Siston AM. / Open Forum Infect Dis. 2015 Dec 28;2(4):ofv164. doi: 10.1093/ofid/ofv164. eCollection 2015 Dec. / https://www.ncbi.nlm.nih.gov/pubmed/26716104

In August 2012, the Chicago Department of Public Health (CDPH) was notified of acute respiratory illness, including 1 fatality, among a group of meeting attendees who stayed at a Chicago hotel during July 30-August 3, 2012. Suspecting Legionnaires' disease (LD), CDPH advised the hotel to close their swimming pool, spa, and decorative lobby fountain and began an investigation. Case finding included notification of individuals potentially exposed during July 16-August 15, 2012. Individuals were interviewed using a standardized questionnaire. An environmental assessment was performed. One hundred fourteen cases were identified: 11 confirmed LD, 29 suspect LD, and 74 Pontiac fever cases. Illness onsets occurred July 21-August 22, 2012. Median age was 48 years (range, 22-82 years), 64% were male, 59% sought medical care (15 hospitalizations), and 3 died. Relative risks for hotel exposures revealed that persons who spent time near the decorative fountain or bar, both located in the lobby were respectively 2.13 (95%, 1.64-2.77) and 1.25 (95% CI, 1.09-1.44) times more likely to become ill than those who did not. Legionella pneumophila serogroup 1 was isolated from samples collected from the fountain, spa, and women's locker room fixtures. Legionella pneumophila serogroup 1 environmental isolates and a clinical isolate had matching sequence-based types. Hotelmaintenance records lacked a record of regular cleaning and disinfection of the fountain. Environmental testing identified Legionella in the hotel's potable water system. Epidemiologic and laboratory data indicated the decorative fountain as the source. Poor fountain maintenance likely created favorable conditions for Legionella overgrowth.

Legionnaires' Disease in Hotels and Passenger Ships: A Systematic Review of Evidence, Sources, and Contributing Factors. / Mouchtouri VA, Rudge JW. / J Travel Med. 2015 Sep-Oct;22(5):325-37. doi: 10.1111/jtm.12225. Epub 2015 Jul 29. Review. / https://www.ncbi.nlm.nih.gov/pubmed/26220258

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 Legionellacontamination 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.

Incidence and risk factors of Legionella pneumophila pneumonia during anti-tumor necrosis factor therapy: a prospective French study. / Lanternier F, Tubach F, Ravaud P, Salmon D, Dellamonica P, Bretagne S, Couret M, Bouvard B, Debandt M, Gueit I, Gendre JP, Leone J, Nicolas N, Che D, Mariette X, Lortholary O; Research Axed on Tolerance of Biotherapies Group. / Chest. 2013 Sep;144(3):990-998. doi: 10.1378/chest.12-2820. / https://www.ncbi.nlm.nih.gov/pubmed/23744173

Our objective was to describe the incidence and risk factors of legionellosis associated with tumor necrosis factor (TNF)-α antagonist use. From February 1, 2004, to January 31, 2007, we prospectively collected all cases of legionellosis among French patients receiving TNF-α antagonists in the Research Axed on Tolerance of Biotherapies (RATIO) national registry. We conducted an incidence study with the French population as a reference and a case-control analysis with four control subjects receiving TNF-α antagonists per case of legionellosis. Twenty-seven cases of legionellosis were reported. The overall annual incidence rate of legionellosis for patients receiving TNF-α antagonists, adjusted for age and sex, was 46.7 (95% CI, 0.0-125.7) per 100,000 patient-years. The overall standardized incidence ratio (SIR) was 13.1 (95% CI, 9.0-19.1; P &lt; .0001) and was higher for patients receiving infliximab (SIR, 15.3 [95% CI, 8.5-27.6; P &lt; .0001]) or adalimumab (SIR, 37.7 [95% CI, 21.9-64.9; P &lt; .0001]) than etanercept (SIR, 3.0 [95% CI, 1.00-9.2; P = .06]). In the case-control analysis, exposure to adalimumab (OR, 8.7 [95% CI, 2.1-35.1]) or infliximab (OR, 9.2 [95% CI, 1.9-45.4]) vs etanercept was an independent risk factor for legionellosis. The incidence rate of legionellosis for patients receiving TNF-α antagonists is high, and the risk is higher for patients receiving anti-TNF-α monoclonal antibodies than soluble TNF-receptor therapy. In case of pneumonia occurring during TNF-α antagonist therapy, specific urine antigen detection should be performed and antibiotic therapy should cover legionellosis.

[Evaluation of a Legionella outbreak emerged in a recently opening hotel]. / Erdoğan H, Arslan H. / Mikrobiyol Bul. 2013 Apr;47(2):240-9. Turkish. Erratum in: Mikrobiyol Bul. 2013 Jul;47(3):570. / https://www.ncbi.nlm.nih.gov/pubmed/23621724

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.

Preliminary report: outbreak of Legionnaires disease in a hotel in Calp, Spain, update on 22 February 2012. / Vanaclocha H, Guiral S, Morera V, Calatayud MA, Castellanos M, Moya V, Jerez G, Gonzalez F. / Euro Surveill. 2012 Feb 23;17(8). pii: 20093. / https://www.ncbi.nlm.nih.gov/pubmed/22401506

Research is ongoing on eighteen cases of Legionellosis, including four deaths, identified among tourists and employees in a hotel in Calp, Spain. Cases occurred during a period of two months, indicating the possibility of a point-source transmission at the hotel. An environmental investigation identified several positive samples in the hotel, which as a precautionary measure, was closed until requested improvements were made. Surveillance measures currently remain active.

In vitro activity of antimicrobial agents against Legionella isolated from environmental water systems: first results from Turkey. / Erdogan H, Can F, Demirbilek M, Timurkaynak F, Arslan H. / Environ Monit Assess. 2010 Dec;171(1-4):487-91. doi: 10.1007/s10661-009-1293-y. Epub 2010 Jan 5. Erratum in: Environ Monit Assess. 2010 Dec;17(1-4):689. / https://www.ncbi.nlm.nih.gov/pubmed/20049525

We evaluated the in vitro activity of antimicrobial agents against Legionella obtained from hotel and hospital water systems in three different regions of Turkey. Sixty-five Legionella strains (Legionella pneumophila serogroup 6 [n=32], L. pneumophila serogroup 1 [n=27], L. pneumophila serogroup 3 [n=2], and Legionella spp. [n=4]) were tested against levofloxacin, ciprofloxacin, clarithromycin, azithromycin, and rifampicin. The minimum inhibitory concentration (MIC) values of each antimicrobial agent for these strains was determined by the microdilution method using buffered yeast extract medium supplemented with 0.1% ketoglutarate broth. L. pneumophila ATCC 33152, Staphylococcus aureus ATCC 29213, and Escherichia coli ATCC 25922 were used as controls. Minimum inhibitory concentration values were in the following ranges: clarithromycin 0.001-0.5 mg/L, azithromycin 0.001-0.5 mg/L, levofloxacin 0.001-0.5 mg/L, ciprofloxacin 0.001-0.125 mg/L, and rifampicin 0.001- 0.5 mg/L. The MIC(90) for rifampicin, levofloxacin, ciprofloxacin, azithromycin, and clarithromycin were 0.015, 0.125, 0.06, 0.125, and 0.06 mg/L, respectively. To the best of our knowledge, this is the first study to determine in vitro activities of antimicrobial agents against Legionella species in Turkey. Rifampicin had the lowest MIC(90) value. It would seem that azithromycin and clarithromycin exhibit good activity as well as levofloxacin and ciprofloxacin against Legionella isolated from environmental water systems in Turkey.

Evaluation of Legionella pneumophila contamination in Italian hotel water systems by quantitative real-time PCR and culture methods. / Bonetta S, Bonetta S, Ferretti E, Balocco F, Carraro E. / J Appl Microbiol. 2010 May;108(5):1576-83. doi: 10.1111/j.1365-2672.2009.04553.x. Epub 2009 Sep 11. / https://www.ncbi.nlm.nih.gov/pubmed/19796090

This study was designed to define the extent of water contamination by Legionella pneumophila of certain Italian hotels and to compare quantitative real-time PCR with the conventional culture method. Nineteen Italian hotels of different sizes were investigated. In each hotel three hot water samples (boiler, room showers, recycling) and one cold water sample (inlet) were collected. Physico-chemical parameters were also analysed. Legionellapneumophila was detected in 42% and 74% of the hotels investigated by the culture method and by real-time PCR, respectively. In 21% of samples analysed by the culture method, a concentration of >10(4) CFU l(-1) was found, and Leg. pneumophila serogroup 1 was isolated from 10.5% of the hotels. The presence of Leg. pneumophila was significantly influenced by water sample temperature, while no association with water hardness or residual-free chlorine was found. This study showed a high percentage of buildings colonized by Leg. pneumophila. Moreover, real-time PCR proved to be sensitive enough to detect lower levels of contamination than the culture method. This study indicates that the Italian hotels represent a possible source of risk for Legionnaires' disease and confirms the sensitivity of the molecular method. To our knowledge, this is the first report to demonstrate Legionella contamination in Italian hotels using real-time PCR and culture methods.

[Prevention of legionellosis in hotel establishments: a proposal to introduce a plan of action in accordance with Provision 13 January 2005 (Italy)]. / Delia S, Laganà P, Minutoli E, Cannavò G, Parisi S. / Ig Sanita Pubbl. 2008 Jul-Aug;64(4):485-507. Italian. Erratum in: Ig Sanita Pubbl. 2009 Mar-Apr;65(2):188. Santi, Delia [corrected to Delia, Santi]. / https://www.ncbi.nlm.nih.gov/pubmed/18985083

Provision 13 January 2005 (Italy) gives guidelines for legionellosis control and prevention in hotel and thermal establishments. Considering that Legionella pneumophila is an ubiquitous organism , the implementation of actions to control the risk of Legionella in the water distribution systems of various types of establishments (hospital, hotel, thermal), or to at least reduce it to acceptable levels, is warranted. The authors have prepared a plan of action for Legionella which, besides describing the main points of the provision and the roles of managers and technicians, also includes the data sheets to be used during environmental monitoring procedures. The action plan will be freely available through local health authorities and professional associations.

European network cooperation to identify hotel as source for pneumonia caused by Legionellapneumophila serogroup 2. / Lück PC, Hahn F, Senger M, Boers SA, Brandsema P. / Euro Surveill. 2008 Jun 12;13(24). pii: 18903. No abstract available. / https://www.ncbi.nlm.nih.gov/pubmed/18761945

Here we describe a case of hotel-associated legionellosis in an immuno-competent man caused byLegionella pneumophila serogroup 2, sequence type (ST) 39 that was identified through European cooperation.

Persistence of chlorine-sensitive Legionella pneumophila in hyperchlorinatedinstallations. / García MT, Baladrón B, Gil V, Tarancon ML, Vilasau A, Ibañez A, Elola C, Pelaz C. / J Appl Microbiol. 2008 Sep;105(3):837-47. doi: 10.1111/j.1365-2672.2008.03804.x. Epub 2008 Jun 14. / https://www.ncbi.nlm.nih.gov/pubmed/18557962

To study the persistence of Legionella over time in different disinfected facilities and analysing whether failures in bacterial eradication could be the result of a decrease in the susceptibility of the persistent strains to subsequent treatments. A long-term environmental surveillance was carried out in three different facilities associated with cases of Legionnaires' disease (a hospital, a fishing boat and a hotel). Despite several hyperchlorination episodes, amplified fragment length polymorphism, pulsed field gel electrophoresis-SfiI and arbitrarily primed polymerase chain reaction methods demonstrated that a specific clone of L. pneumophila serogroup 1 was able to survive for 17, 5 and 10 years in the hospital, fishing boat and the hotel, respectively. Isolates from different years from the same facility showed similar minimal inhibitory concentration and minimal bactericidal concentration values against eight different disinfectants. Hyperchlorination over long periods of time did not prevent the persistence of L. pneumophila. The lack of effectiveness did not appear to be the result of a decreased susceptibility of Legionella to chlorine. Hyperchlorination did not modify in vitro susceptibility of Legionella to other disinfectants to which the bacteria had not previously been exposed.

Colonization of Legionella species in hotel water systems in Turkey. / Erdogan H, Arslan H. / J Travel Med. 2007 Nov-Dec;14(6):369-73. / https://www.ncbi.nlm.nih.gov/pubmed/17995531

The goal of this study was to evaluate the prevalence of Legionella species in hotel water distribution systems in Alanya, Turkey, which is an important tourism center. Water and swab samples were obtained from 52 Turkish hotels from August 2003 to September 2005. Water samples were collected in 100 mL sterile containers and were concentrated by membrane filters with a pore size of 0.45 microm. Heat treatment was used to eliminate other microorganisms from the samples, which were then spread on buffered charcoal yeast extract alpha agar plates and glycine, vancomycin, polymyxin, cycloheximide agar plates. Cysteine-dependent colonies were identified by latex agglutination. In all, 491 water and swab samples were analyzed. The results of all samples were negative for Legionella in 16 (30.8%) hotels. Legionella species (92.5% of which were Legionella pneumophila) were detected in 93 (18.9%) of the samples. The most frequently isolated species were L pneumophila serogroups 6 (63.5%) and 1 (21.5%). Legionella pneumophila serogroup 6 was the most common isolate detected in Turkish hotel water systems in our study. The result of Legionella urinary antigen tests, which are the diagnostic tests most often used to identify legionnaires' disease, may be negative in people infected with L pneumophila serogroup 6. We suggest that clinicians should apply the whole spectrum of laboratory methods for the detection of legionnaires' disease in patients with pneumonia of unknown origin and history of travel to Alanya, Turkey.

Microbiological quality of indoor and outdoor swimming pools in Greece: investigation of the antibiotic resistance of the bacterial isolates. / Papadopoulou C, Economou V, Sakkas H, Gousia P, Giannakopoulos X, DontorouC, Filioussis G, Gessouli H, Karanis P, Leveidiotou S. / Int J Hyg Environ Health. 2008 Jul;211(3-4):385-97. Epub 2007 Aug 28. / https://www.ncbi.nlm.nih.gov/pubmed/17728184

During 1997-2005, the microbiological quality and susceptibility of bacterial isolates of swimming pool waters were investigated. A total of 462 water samples were collected from three indoor swimming pools (a teaching pool, a competition public pool, a hydrotherapy pool) and two outdoor swimming pools (a hotel semi-public and a residential private pool) in Northwestern Greece. All water samples were analyzed for the presence of bacteria, protozoa and fungi and susceptibility tests were performed for the bacterial isolates. Sixty-seven percent of the examined water samples conformed to the microbiological standards and 32.9% exceeded at least one of the indicated limits. Out of 107 bacterial isolates, 38 (35.5%) resistant strains were detected. Multi-resistant Pseudomonas alcaligenes, Leuconostoc, and Staphylococcus aureus (isolated from the teaching pool), Staphylococcus wernerii, Chryseobacterium indologenes and Ochrobactrum anthropi (isolated from the competition pool), Pseudomonas aeruginosa, P. fluorescens, Aeromonas hydrophila, Enterobacter cloacae, Klebsiella pneumoniae and S. aureus (isolated from the hydrotherapy pool) and A. hydrophila (isolated from the hotel pool) were detected. The swimming pool with the poorest microbiological quality (THC 500 cfu/ml in 12.1% of the samples, P. aeruginosa counts 1500 cfu/100 ml in 6% of the samples) and the highest prevalence of multi-resistant isolates (73.6%) was the hydrotherapy pool. No Cryptosporidium or Giardia cysts and no Legionella, Mycobacteria and Salmonella were detected, but there were isolations of Candida albicans, Aspergillus spp., Mucor spp., Alternaria spp., Rhizopus spp., Trichophyton spp., and Penicillium spp.

Risk factors for contamination of hotel water distribution systems by Legionella species. / Mouchtouri V, Velonakis E, Tsakalof A, Kapoula C, Goutziana G, Vatopoulos A, Kremastinou J, Hadjichristodoulou C. / Appl Environ Microbiol. 2007 Mar;73(5):1489-92. Epub 2007 Jan 19. / https://www.ncbi.nlm.nih.gov/pubmed/17261527

The Legionella colonization frequency at 385 Greek hotel hot and cold water distribution systems was 20.8%. Legionella contamination was associated with the presence of an oil heater (odds ratio [OR]=2.04, 95% confidence interval [CI]=1.12 to 3.70), with the sample temperature (OR=0.26, 95% CI=0.1 to 0.5), with seasonal operation (OR=3.23, 95% CI=1.52 to 6.87), and with the presence of an independent disinfection system (OR=0.30, 95% CI=0.15 to 0.62). The same water temperatures, free-chlorine levels, and pHs differently affect the survival of various Legionella spp.

A large, travel-associated outbreak of legionellosis among hotel guests: utility of the urine antigen assay in confirming Pontiac fever. / Burnsed LJ, Hicks LA, Smithee LM, Fields BS, Bradley KK, Pascoe N, Richards SM, Mallonee S, Littrell L, Benson RF, Moore MR; Legionellosis Outbreak Investigation Team. / Clin Infect Dis. 2007 Jan 15;44(2):222-8. Epub 2006 Dec 8. / https://www.ncbi.nlm.nih.gov/pubmed/17173221

During March 2004, a large outbreak of legionnaires disease and Pontiac fever occurred among hotel guests in Oklahoma. An investigation was conducted to identify the source and evaluate the utility of the Legionella urine antigen assay and serologic testing for the identification of Pontiac fever. A retrospective cohort investigation of hotel guests and employees and an environmental evaluation were performed. Participants were interviewed, and clinical specimens were collected from consenting individuals. Six cases of legionnaires disease and 101 cases of Pontiac fever were identified. Exposure to the indoor pool and hot tub area was associated with legionellosis (relative risk, 4.4; 95% confidence interval, 2.8-6.9). Specimens from the pool and hot tub tested positive for Legionella pneumophila serogroup 1 by polymerase chain reaction. For Pontiac fever, the sensitivity and positive predictive value were 35.7% and 100%, respectively, for the urine antigen assay, and 46.4% and 90%, respectively, for serologic testing. The specificity and negative predictive value were 100% and 47.8%, respectively, for the urine antigen assay, and 89.3% and 45.5%, respectively, for serologic testing. Urine antigen testing, with or without serologic testing, can be used to confirm outbreak-associated cases of Pontiac fever caused by L. pneumophila serogroup 1.

Legionella prevalence in hot spring recreation areas of Taiwan. / Hsu BM, Chen CH, Wan MT, Cheng HW. / Water Res. 2006 Oct;40(17):3267-73. Epub 2006 Aug 22. / https://www.ncbi.nlm.nih.gov/pubmed/16928391

Legionella is a bacterium ubiquitous to aquatic environments. Within the genus a few species are recognized as opportunistic potential human pathogens, especially the species Legionella pneumophila, which causes pneumonia legionellosis. Outbreaks of legionellosis are frequently reported by hotel guests and hospital patients, and are spread through inhaled aerosols of contaminated institutional water systems. Contaminations in hot tubs, spas and public baths are also possible. As a result, in this study, we investigated the distribution of Legionella at seven hot spring recreational areas throughout Taiwan. We gathered data on factors potentially associated with the pathogen's distribution, including environment, facility operation, and physical and microbiological water quality parameters. Spring water was collected from 91 sites and Legionella was detected in 21 (23%). The most frequently detected was L. pneumophila, followed by uncultured Legionellaspecies, Legionella-like amoebal pathogen. Five species, L. bozemanii, L. dumoffi, L. feelei, L. lyticum and L. oakridgenesis, were all detected once. Legionella species were found in water temperatures ranging from 22 to 50 degrees C. Optimal pH appeared to be between 5.0 and 9.0. The prevalence of Legionella also coincided with the prevalence of indicator microorganisms. Legionella detection was not proportional to the frequency of cleaning. Results of this survey confirm the ubiquity of Legionella in Taiwan spring recreation areas. L. pneumophila, the organism responsible for the majority of legionellosis outbreaks, should be considered a potential public health threat in spa areas of Taiwan.

Legionella contamination in hot water of Italian hotels. / Borella P, Montagna MT, Stampi S, Stancanelli G, Romano-Spica V, Triassi M, Marchesi I, Bargellini A, Tatò D, Napoli C, Zanetti F, Leoni E, Moro M, Scaltriti S, Ribera D'Alcalà G, Santarpia R, Boccia S. / Appl Environ Microbiol. 2005 Oct;71(10):5805-13. / https://www.ncbi.nlm.nih.gov/pubmed/16204491

A cross-sectional multicenter survey of Italian hotels was conducted to investigate Legionella spp. contamination of hot water. Chemical parameters (hardness, free chlorine concentration, and trace element concentrations), water systems, and building characteristics were evaluated to study risk factors for colonization. The hot water systems of Italian hotels were strongly colonized by Legionella; 75% of the buildings examined and 60% of the water samples were contaminated, mainly at levels of > or =10(3) CFU liter(-1), and Legionellapneumophila was the most frequently isolated species (87%). L. pneumophila serogroup 1 was isolated from 45.8% of the contaminated sites and from 32.5% of the hotels examined. When a multivariate logistic model was used, only hotel age was associated with contamination, but the risk factors differed depending on the contaminating species and serogroup. Soft water with higher chlorine levels and higher temperatures were associated with L. pneumophila serogroup 1 colonization, whereas the opposite was observed for serogroups 2 to 14. In conclusion, Italian hotels, particularly those located in old buildings, represent a major source of risk for Legionnaires' disease due to the high frequency of Legionella contamination, high germ concentration, and major L. pneumophila serogroup 1 colonization. The possible role of chlorine in favoring the survival of Legionella species is discussed.

Outbreak of travel-related pontiac fever among hotel guests illustrating the need for better diagnostic tests. / Huhn GD, Adam B, Ruden R, Hilliard L, Kirkpatrick P, Todd J, Crafts W, Passaro D, Dworkin MS. / J Travel Med. 2005 Jul-Aug;12(4):173-9. / https://www.ncbi.nlm.nih.gov/pubmed/16086890

Pontiac fever (PF), a legionellosis with influenza-like symptoms and high attack rates, is rarely reported. Travel-related outbreaks can elude detection because infected persons are often widely removed geographically from the transmission source before illness onset. Thirty-one persons staying at an Illinois hotel during August 9 to 11, 2002, reported influenza-like symptoms to local health departments within 24 to 48 hours of checkout. We investigated to identify the cause and source of illness to guide control measures. Hotel water samples were collected for culture. A telephone questionnaire detailing illness symptoms and exposures was administered to all who were guests at the hotel from August 9 to 15 (n = 380). A case was defined as onset of fever, headache, and myalgia in a guest in the 14 days following the hotel stay. Patient sera were tested by hemagglutination assay for antibodies to Legionella species. Among 204 questionnaire respondents from 15 states and Canada, 50 met the case definition. Among persons exposed to the swimming pool/whirlpool spa area, 63% (47 of 75) became ill versus 3% (3 of 110) of unexposed persons (relative risk 23.0, 95% CI 7.4-71.1). Illness risk increased with increasing time exposed to the pool/spa. Approximately 95 to 115 bathers per day, two to three times above the usual number, used the spa during August 9 to 11. Three Legionella species, L. dumoffii, L. maceachernii, and L. micdadei, were isolated from spa filter backwash cultures. Two of 15 ill persons with acute- and convalescent-phase sera had a greater than fourfold rise in antibody titer to L. micdadei. PF was associated with exposure to a hotel pool/spa area. Heavy bather usage likely contributed to a decreased effectiveness of the disinfectant in the whirlpool spa, possibly promoting bacterial aerosolization. Linking case information from many states is essential in identifying and eliminating the source of disease transmission in travel-related outbreaks of PF. Clinicians should be aware of PF in the differential diagnosis of patients with influenza-like symptoms following recent travel, particularly with exposure to a communal-use whirlpool spa.

Recurrence of legionnaires disease at a hotel in the United States Virgin Islands over a 20-year period. / Cowgill KD, Lucas CE, Benson RF, Chamany S, Brown EW, Fields BS, Feikin DR. / Clin Infect Dis. 2005 Apr 15;40(8):1205-7. Epub 2005 Mar 3. / https://www.ncbi.nlm.nih.gov/pubmed/15791524

We investigated 3 cases of legionnaires disease (LD) that developed in travelers who stayed at a hotel in the United States Virgin Islands where cases of LD occurred in 1981-1982 and in 1998. The temperature of the potable water at the hotel was in a range that could optimally support the growth of Legionella species, and the potable water was colonized with Legionella pneumophila in 1981-1982 and in 2002-2003.

Legionnaires disease associated with potable water in a hotel--Ocean City, Maryland, October 2003-February 2004. / Centers for Disease Control and Prevention (CDC). / MMWR Morb Mortal Wkly Rep. 2005 Feb 25;54(7):165-8. / https://www.ncbi.nlm.nih.gov/pubmed/15729216

During October 2003-February 2004, eight cases (seven confirmed cases and one possible) of Legionnaires disease (LD) were identified among guests at a hotel in Ocean City, Maryland. This report summarizes the subsequent investigation conducted by the Worcester County Health Department (WCHD), Maryland Department of Health and Mental Hygiene (DHMH), and CDC, which implicated the potable hot water system of the hotel as the most likely source of infection. The detection of this outbreak underscores the importance of enhanced, state-based surveillance for timely detection of travel-associated LD and implementation of control measures.

Legionella waterline colonization: detection of Legionella species in domestic, hotel and hospital hot water systems. / Leoni E, De Luca G, Legnani PP, Sacchetti R, Stampi S, Zanetti F. / J Appl Microbiol. 2005;98(2):373-9. / https://www.ncbi.nlm.nih.gov/pubmed/15659192

An evaluation was made of the prevalence of Legionella species in hot water distribution systems in the city of Bologna (Italy) and their possible association with bacterial contamination (total counts and Pseudomonadaceae) and the chemical characteristics of the water (pH, Ca, Mg, Fe, Mn, Cu, Zn and Total Organic Carbon, TOC). A total of 137 hot water samples were analysed: 59 from the same number of private apartments, 46 from 11 hotels and 32 from five hospitals, all using the same water supply. Legionella species were detected in 40.0% of the distribution systems, L. pneumophila in 33.3%. The highest colonization was found in the hot water systems of hospitals (93.7% of samples positive for L. pneumophila, geometric mean: 2.4 x 10(3) CFU l(-1)), followed by the hotels (60.9%, geometric mean: 127.3 CFU l(-1)) and the apartments with centralized heating (41.9%, geometric mean: 30.5 CFU l(-1)). The apartments with independent heating systems showed a lower level of colonization (3.6% for Legionella species), with no evidence of L. pneumophila. Correlation analysis suggests that copper exerts an inhibiting action, while the TOC tends to favour the development of L. pneumophila. No statistically significant association was seen with Pseudomonadaceae, which were found at lower water temperatures than legionellae and in individual distribution points rather than in the whole network. The water recirculation system used by centralized boilers enhances the spreading of legionellae throughout the whole network, both in terms of the number of colonized sites and in terms of CFU count. Differences in Legionella colonization between types of buildings are not due to a variation in water supply but to other factors. Besides the importance of water recirculation, the study demonstrates the inhibiting action of copper and the favourable action of TOC on the development of L. pneumophila.

European Guidelines for Control and Prevention of Travel Associated Legionnaires' Disease: the Italian experience. / Rota MC, Caporali MG, Massari M; European Working Group for Legionella Infections. / Euro Surveill. 2004 Feb;9(2):10-1. / https://www.ncbi.nlm.nih.gov/pubmed/15010572

In Italy, 35 clusters of travel associated Legionnaires' disease were identified from July 2002, when the European Guidelines for Control and Prevention of Travel Associated Legionnaires' Disease have been adopted by the EWGLINET network, to October 2003. Eight per cent (28.6%) would not have been identified without the network. The clusters detected were small, ranging from 2 cases to a maximum of 6. All clusters involved 5 camping sites and 30 hotels/residences, and an overall of 87 patients. The diagnosis was confirmed in 92.0% of the cases and mainly performed by urinary antigen detection (84.7%). A clinical isolate was available only in one case. Following environmental investigations, samples were collected for all the 35 clusters from the water system, and Legionella pneumophila was found in 23 occasions (65.7%). In 15 resorts out of 35, investigations were already in progress at the time of EWGLI cluster notification, since in Italy full environmental investigation is performed even after notification of a single case. Control measures were implemented in all accommodation sites at risk and one hotel only was closed. In all the 35 clusters, reports were completed and sent on time, highlighting that it is possible to comply with the procedures requested by the European Guidelines.

[Legionellosis, a tourist problem?]. / Kistler W, Fleisch F, Reinhart WH, Wieland T. / Praxis (Bern 1994). 2002 Jul 31;91(31-32):1241-5. German. / https://www.ncbi.nlm.nih.gov/pubmed/12212344

Legionellosis is a relatively rare disease characterized by an often prolonged and complicated course even in immunocompetent patients. Its diagnosis is mandatory for therapeutic and epidemiologic reasons. At the Kantonsspital Chur between 1998 and 2001, 6 cases of legionellosis have been observed: four of them were travel-associated and one concerned a local hotel employee. Due to the increasing international mobility epidemiologic investigations for the localization and elimination of the sources of infection are very difficult. A european task force, the European Working Group for Legionella Infections (EWGLI/www.ewgli.org) is addressing this problem. It is a matter of debate to what extent the public should be informed about sources of legionellosis (so called legionella hotels).

Pneumonia involving Legionella pneumophila and Listeria monocytogenes in an immunocompromised patient: an unusual coinfection. / Lerolle N, Zahar JR, Duboc V, Tissier F, Rabbat A. / Respiration. 2002;69(4):359-61. / https://www.ncbi.nlm.nih.gov/pubmed/12169753

[Studies on Legionella-contamination to the air-conditioning cooling towers in big hotels and on its seroprevalence in the related populations in Beijing]. / Peng X, Pei H, Li X, He X, Yang A, Tang Y, Cao R. / Zhonghua Liu Xing Bing Xue Za Zhi. 2000 Aug;21(4):289-91. Chinese. / https://www.ncbi.nlm.nih.gov/pubmed/11860803

An outbreak of travel-associated Legionnaires disease and Pontiac fever: the need for enhanced surveillance of travel-associated legionellosis in the United States. / Benin AL, Benson RF, Arnold KE, Fiore AE, Cook PG, Williams LK, Fields B, Besser RE. / J Infect Dis. 2002 Jan 15;185(2):237-43. Epub 2001 Dec 18. / https://www.ncbi.nlm.nih.gov/pubmed/11807698

Pontiac fever due to Legionella micdadei from a whirlpool spa: possible role of bacterial endotoxin. / Fields BS, Haupt T, Davis JP, Arduino MJ, Miller PH, Butler JC. / J Infect Dis. 2001 Nov 15;184(10):1289-92. Epub 2001 Oct 2. / https://www.ncbi.nlm.nih.gov/pubmed/11679917

A small outbreak of Legionnaires' disease in a cargo ship under repair. / Caylà JA, Maldonado R, González J, Pellicer T, Ferrer D, Pelaz C, Gracia J, Baladrón B, Plaséncia A; Legionellosis study group. / Eur Respir J. 2001 Jun;17(6):1322-7. / https://www.ncbi.nlm.nih.gov/pubmed/11491180

[Legionellas in domestic warm water--effects on the health of residents]. / Heudorf U, Hentschel W, Hoffmann M, Lück C, Schubert R. / Gesundheitswesen. 2001 May;63(5):326-34. German. / https://www.ncbi.nlm.nih.gov/pubmed/11441676

A whirlpool associated outbreak of Pontiac fever at a hotel in Northern Sweden. / Götz HM, Tegnell A, De Jong B, Broholm KA, Kuusi M, Kallings I, Ekdahl K. / Epidemiol Infect. 2001 Apr;126(2):241-7. / https://www.ncbi.nlm.nih.gov/pubmed/11349975

First isolation of Legionella pneumophila in Sri Lanka. / Wahala WM, Wickramasinghe RS. / Ceylon Med J. 2000 Dec;45(4):171-2. / https://www.ncbi.nlm.nih.gov/pubmed/11293965

Legionella from guests of Welsh hotel indistinguishable from humidifier isolates. / [No authors listed] / Commun Dis Rep CDR Wkly. 2000 Apr 21;10(16):141. No abstract available. / https://www.ncbi.nlm.nih.gov/pubmed/10826219

[Legionnaires' disease in travellers]. / Jarraud S, Reyrolle M, Riffard S, Lo Presti F, Etienne J. / Bull Soc Pathol Exot. 1998;91(5 Pt 1-2):486-9. French. / https://www.ncbi.nlm.nih.gov/pubmed/10078391

A simple method for the eradication of Legionella pneumophila from potable water systems. / Moreno C, de Blas I, Miralles F, Apraiz D, Catalan V. / Can J Microbiol. 1997 Dec;43(12):1189-96. / https://www.ncbi.nlm.nih.gov/pubmed/9476354

[Description and study of the etiology of a community outbreak of atypical pneumonia in L'Espluga de Francolí, Tarragona]. / Ramon Duch F, Ruiz de Porras L, Elizalde G, Abellà M. / Med Clin (Barc). 1997 Apr 5;108(13):490-4. Spanish. / https://www.ncbi.nlm.nih.gov/pubmed/9235425

An international investigation of an outbreak of Legionnaires disease among UKand French tourists. / Joseph C, Morgan D, Birtles R, Pelaz C, Martín-Bourgón C, Black M, Garcia-Sanchez I, Griffin M, Bornstein N, Bartlett C. / Eur J Epidemiol. 1996 Jun;12(3):215-9. / https://www.ncbi.nlm.nih.gov/pubmed/8884186

Legionellosis linked with a hotel car park--how many were infected? / Bell JC, Jorm LR, Williamson M, Shaw NH, Kazandjian DL, Chiew R, Capon AG. / Epidemiol Infect. 1996 Apr;116(2):185-92. / https://www.ncbi.nlm.nih.gov/pubmed/8620910

Subtyping of Legionella pneumophila isolates by arbitrarily primed polymerase chain reaction. / Ledesma E, Camaró ML, Carbonell E, Sacristán T, Martí A, Pellicer S, Llorca J, Herrero P, Dasí MA. / Can J Microbiol. 1995 Sep;41(9):846-8. / https://www.ncbi.nlm.nih.gov/pubmed/7585361

[Genomic DNA fingerprints of Legionella pneumophila serogroup 2 strains as an epidemiologic marker]. / Bender-Beck L, Mühlenberg W, Lück PC, Ott M, Horbach I, Fehrenbach FJ, Wewalka G, Hacker J. / Immun Infekt. 1995 Aug;23(4):137-9. German. / https://www.ncbi.nlm.nih.gov/pubmed/7558118

[Fatal travel-associated legionella infection caused by shower aerosols in a German hotel]. / Mühlenberg W. / Gesundheitswesen. 1993 Dec;55(12):653-6. German. / https://www.ncbi.nlm.nih.gov/pubmed/8111164

Outbreak of Legionnaire's disease linked to a decorative fountain by molecular epidemiology. / Hlady WG, Mullen RC, Mintz CS, Shelton BG, Hopkins RS, Daikos GL. / Am J Epidemiol. 1993 Oct 15;138(8):555-62. / https://www.ncbi.nlm.nih.gov/pubmed/8237978

[A report on investigation of an outbreak of Legionnaires' disease in a hotel in Beijing]. / Deng C. / Zhonghua Liu Xing Bing Xue Za Zhi. 1993 Apr;14(2):78-80. Chinese. / https://www.ncbi.nlm.nih.gov/pubmed/8353821

In-vitro activity of RP 59500, a new synergic antibacterial agent, against Legionella spp. / Dubois J, Joly JR. / J Antimicrob Chemother. 1992 Jul;30 Suppl A:77-81. / https://www.ncbi.nlm.nih.gov/pubmed/1399954

Incrimination of an environmental source of a case of Legionnaires' disease by pyrolysis mass spectrometry. / Sisson PR, Freeman R, Lightfoot NF, Richardson IR. / Epidemiol Infect. 1991 Aug;107(1):127-32. / https://www.ncbi.nlm.nih.gov/pubmed/1879479

[10 years of legionellosis in Italy (June 1980-June 1990)]. / Castellani Pastoris M, Benedetti P, Greco D. / Ann Ist Super Sanita. 1991;27(2):289-95. Italian. / https://www.ncbi.nlm.nih.gov/pubmed/1755582

Outbreak of Pontiac fever due to Legionella anisa. / Fenstersheib MD, Miller M, Diggins C, Liska S, Detwiler L, Werner SB, Lindquist D, Thacker WL, Benson RF. / Lancet. 1990 Jul 7;336(8706):35-7. / https://www.ncbi.nlm.nih.gov/pubmed/1973219

Role of air sampling in investigation of an outbreak of legionnaires' disease associated with exposure to aerosols from an evaporative condenser. / Breiman RF, Cozen W, Fields BS, Mastro TD, Carr SJ, Spika JS, Mascola L. / J Infect Dis. 1990 Jun;161(6):1257-61. / https://www.ncbi.nlm.nih.gov/pubmed/2345305

Epidemiologic studies have suggested that legionnaires' disease can be transmitted to susceptible hosts by contaminated aerosolized water from cooling towers and evaporative condensers; however, epidemic strains of Legionella have not been isolated by air sampling at such sites during epidemiologic investigations. An outbreak of legionnaires' disease occurred at a retirement hotel; Legionella pneumophila serogroup 1 was isolated from an evaporative condenser and from potable water. A case-control study showed that the only significant exposure risk was in area A. L. pneumophila serogroup 1 was isolated during air sampling near the evaporative condenser exhaust site, the air conditioning intake vent, and an air vent in area A, but not in shower stalls. Monoclonal antibody subtype patterns of L. pneumophila serogroup 1 isolates from patients matched those from the evaporative condenser but not from shower water. Air sampling and monoclonal antibody subtyping results support epidemiologic evidence that the evaporative condenser was the source of this outbreak.

Incidence of Legionella pneumophila infection in tourists: Italy. / Passi C, Maddaluno R, Pastoris MC. / Public Health. 1990 May;104(3):183-8. / https://www.ncbi.nlm.nih.gov/pubmed/2359837

Legionella pneumophila has frequently been recognised as a cause of infection in tourists. From 1973 to 1987, 117 cases of legionellosis were reported in tourists who spent one or more weeks in Italian summer resorts. 6 (5.1%) patients died. 42 (35.9%) were sporadic cases, and 75 (64.1%) were related to clusters or outbreaks. Among the 117 cases, 63 were reported to the Istituto Superiore di Sanità by the health authorities of other countries. Some travellers became ill while in Italy, others soon after they returned home. All tourists but two had stayed in hotels. L. pneumophila was isolated from the water system of 10 hotels, and in another hotel the same Legionella species was detected by direct immunofluorescence. Persistent and/or recurrent sources of infection seem to be present in some summer resorts on the Adriatic Coast and in the Lake Garda area in northern Italy. Some groups of cases were associated with particular hotels over a period of several months and sometimes years. Investigations have implicated potable water as the likely vehicle and the source of infection for tourists. The need of a greater awareness amongst clinicians that travel is a risk factor for legionellosis, and for better international surveillance and cooperation, is stressed.

[An epidemic of legionellosis at a hotel at the Makarska seashore]. / Klismanić-Nuber Z, Milas I, Smoljanović M, Sarić M, Gjenero-Margan I. / Lijec Vjesn. 1990 May-Jun;112(5-6):152-5. Croatian. / https://www.ncbi.nlm.nih.gov/pubmed/2233111

The paper describes the epidemic of Legionellosis that occurred among guests and employees of a hotel at the Makarska littoral in May 1988. According to the so far reported data in the medical literature that was the third epidemic in our country and all three of them occurred in the Dalmatian touristic area. In this epidemic, nine foreign tourists were registered ill with the clinical picture of Legionnaires' disease. Five patients required hospitalization. The disease could be serologically proved in 4 patients and Legionella pneumophila SG1 was isolated from samples of 2 patients and from sediment of the hot-water tank. Since the opening of the hotel until the end of May, 19 hotel employees developed a febrile illness of short duration. The disease was serologically proved in 7 of them. The morbidity rate in tourists was 2.5%, while it amounted to 7.1% in the hotel employees. The epidemic lasted for 16 days. The infection spread through the hot water, and antiepidemic measures were limited to its pasteurization and hyperchloridation. The chain of infection was broken off by the application of those measures.

In vitro activity of lomefloxacin (SC 47111 or NY-198) against isolates of Legionella spp. / Dubois J, Joly JR. / Diagn Microbiol Infect Dis. 1989 May-Jun;12(3 Suppl):89S-91S. / https://www.ncbi.nlm.nih.gov/pubmed/2791504

The in vitro activity of lomefloxacin (SC-47111 or NY-198) was compared with those of erythromycin and rifampin against a total of 180 Legionella spp. strains isolated from nosocomial or acquired respiratory tract infections and from environmental sources. Rifampin was the most active agent tested (MIC90, 0.008 microgram/ml) against Legionella spp. However, lomefloxacin was found 2-to-4-fold more active than erythromycin against most Legionella strains tested. Against Legionella pneumophila, lomefloxacin (MIC90, 0.12 microgram/ml) was significantly more than erythromycin (MIC90, 0.5 micrograms/ml). L. pneumophila serogroup 2, 3, and 5 strains (MIC90, 0.06 micrograms/ml) were more susceptible than L. pneumophila serogroup 1, 4, 6, 7, and 8 (MIC90, 0.12 microgram/ml). L. dumoffii was the most resistant species with a MIC90 of 0.25 microgram/ml and 0.5 microgram/ml, respectively, to lomefloxacin and erythromycin. The activity of lomefloxacin was similar against the isolates obtained from patients or from environmental sources.

[An epidemic of legionnaires' disease in a hotel]. / Gjenero-Margan I, Drazenović V, Vrbica J, Vjerda R, Aleraj B, Borcić B. / Lijec Vjesn. 1989 Mar;111(3):81-4. Croatian. / https://www.ncbi.nlm.nih.gov/pubmed/2747409

An outbreak of legionnaires' disease and epidemic control measures taken at one of our hotels are described. Twenty (1% morbidity) hotelguests were affected with one dying. As a result of field investigations and survey the hot water supply system has been identified as the source of infection. Control measures which created conditions unfavourable to Legionella growth and replication in the hot water system stopped the outbreak.

Lochgoilhead fever: outbreak of non-pneumonic legionellosis due to Legionella micdadei. / Goldberg DJ, Wrench JG, Collier PW, Emslie JA, Fallon RJ, Forbes GI, McKay TM, Macpherson AC, Markwick TA, Reid D. / Lancet. 1989 Feb 11;1(8633):316-8. / https://www.ncbi.nlm.nih.gov/pubmed/2563467

Analysis of case histories from 187 people who had visited a hotel and leisure complex in Lochgoilhead, a village on the west coast of Scotland, indicated that 170 had had an acute illness characterised by headache, fatigue, arthralgia, myalgia, cough, and breathlessness. These symptoms were consistent with Pontiac fever-like illness. Legionella micdadei was isolated from the leisure complex whirlpool spa at the time that 60 of 72 individuals with symptoms seroconverted to L micdadei antigen. This outbreak is thought to be the first of a Pontiac fever-like illness ascribed to L micdadei and the first large-scale outbreak of its kind to have occurred outside North America. Whirlpool spas can be a major reservoir of legionella organisms; they must therefore be properly maintained and operated to prevent outbreaks of infection.

[Legionella pneumophila infection in hotel Aktizeus in Heraklion on Crete?]. / Bijkerk H. / Ned Tijdschr Geneeskd. 1989 Jan 28;133(4):182-3. Dutch. No abstract available. / https://www.ncbi.nlm.nih.gov/pubmed/2922085

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[Legionella pneumophila infection in hotel guests: showers as a probable source of infection]. / Ollé Goig JE, Martín Casabona N, González Fuente T. / Med Clin (Barc). 1987 Feb 21;88(7):261-3. Spanish. No abstract available. / https://www.ncbi.nlm.nih.gov/pubmed/3561070

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Legionnaires' disease in the Caribbean. An outbreak associated with a resort hotel. / Schlech WF 3rd, Gorman GW, Payne MC, Broome CV. / Arch Intern Med. 1985 Nov;145(11):2076-9. / https://www.ncbi.nlm.nih.gov/pubmed/4062461

Outbreaks of legionnaires' disease (LD) in tourists visiting Italian and Spanish resorts have been recently reported. An unusual number of reports of LD in tourists visiting the US Virgin Islands prompted an investigation of risk factors for development of LD in this area. Twenty-seven cases of LD were identified between 1979 and 1982 through press reports, personal communication, the national LD surveillance system, a review of hospital records, and a mail survey. Twenty-four of 27 persons with the disease had visited St Croix and 12 of them had stayed at a single hotel in 1981. Available evidence suggested that infection was due to Legionella pneumophila serogroup 1; L pneumophila serogroups 1 and 3 and several new Legionella species were isolated from the potable water system at the hotel. Following hyperchlorination of the potable water system, no further cases of LD in hotel visitors have been identified to date.

[Legionnaires' disease among Dutch tourists in a hotel in Pineda de Mar, Spain]. / Bijkerk H, van Os M. / Ned Tijdschr Geneeskd. 1985 May 11;129(19):918-20. Dutch. No abstract available. / https://www.ncbi.nlm.nih.gov/pubmed/4010801

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Febrile illness in successive cohorts of tourists at a hotel on the Italian Adriatic coast: evidence for a persistent focus of Legionella infection. / Rosmini F, Castellani-Pastoris M, Mazzotti MF, Forastiere F, Gavazzoni A, Greco D, Ruckdeschel G, Tartagni E, Zampieri A, Baine WB. / Am J Epidemiol. 1984 Jan;119(1):124-34. / https://www.ncbi.nlm.nih.gov/pubmed/6691329

Outbreaks of febrile illness consistent with legionellosis occurred in successive groups of vacationers at an Adriatic resort in 1980. Illness was associated with one of two hotels used by the groups. A cohort study of guests of the suspect hotel revealed 23 cases of febrile illness with pulmonary symptoms, significant antibody titers to Legionella pneumophila, or both, among 291 persons at risk. Two patients died. Attack rates ranged from 0-19% in the nine cohorts of vacationers and were highest among the most elderly. Febrile illness in the last two cohorts of the season was associated with an antibody titer greater than or equal to 128. L. pneumophila was isolated from shower heads in the suspect hotel, but no association was found between showering and illness or seropositivity. Bacteria identified as L. pneumophila by direct immunofluorescence were also found in water from an adjacent hotel and from the outflow from a common well. No cases were associated with the adjacent hotel.

Legionella in hospital and hotel water supplies. / Bartlett CL, Kurtz JB, Hutchison JG, Turner GC, Wright AE. / Lancet. 1983 Dec 3;2(8362):1315. No abstract available. / https://www.ncbi.nlm.nih.gov/pubmed/6139664

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Direct demonstration and isolation of Legionella pneumophila (serogroup 1) from bathroom water specimens in a hotel. / Sethi KK, Brandis H. / Zentralbl Bakteriol Mikrobiol Hyg B. 1983 Jun;177(5):402-5. / https://www.ncbi.nlm.nih.gov/pubmed/6367308

Legionella pneumophila serogroup 1 organisms were isolated from one sample of water originating from a shower head in a bathroom of a hotel. Seven of the 16 swab specimens collected from 2 different sites of the hotel bathrooms revealed fluorescing bacteria in direct fluorescent antibody test. The significance of present observations in relation to the cluster of L. pneumophila infections diagnosed recently in Berlin among a group of visitors who stayed in this hotel has been discussed.

Epidemic Legionnaires' disease. Airborne transmission down a chimney. / Band JD, LaVenture M, Davis JP, Mallison GF, Skaliy P, Hayes PS, Schell WL, Weiss H, Greenberg DJ, Fraser DW. / JAMA. 1981 Jun 19;245(23):2404-7. / https://www.ncbi.nlm.nih.gov/pubmed/7230470

Between June 18 and July 9, 1979, Legionnaires' disease (LD) developed in 13 persons who had visited a hotel complex in Wisconsin. All had visited the part of the hotel that contains the restaurants and meeting rooms (building A). Legionnaires' disease occurred in 1% who had been exclusively in the meeting rooms and in 0.1% who had eaten only at the hotel restaurants. Furthermore, 1.5% exposed to meeting room 1 and none of those exposed only to the other meeting rooms had LD. Legionella pneumophila was isolated from water in the cooling tower on top of building A. Located within 5 m downwind of the cooling-tower exhaust, a chimney with an open damper allowed cooling-tower exhaust (as demonstrated by air tracer studies) to enter meeting room 1 via the fireplace. Although cases did not occur after the cooling-tower water was treated by continuous hyperchlorination and the chimney was sealed, a seven-day lag occurred between treatment and elimination of the organism from the tower water.

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