1.1 Description of disease
Legionella infection or legionellosis can manifest clinically in two ways:
- Legionnaires’ disease: a severe, potentially fatal form of pneumonia usually resulting in hospitalisation which is characterised by myalgia, fever and cough.
- Pontiac fever: a milder form of disease characterised by flu-like symptoms but pneumonia is not present.
Both diseases are caused by bacteria from the Legionella species which are ubiquitous in both natural and artificial aquatic environments. Legionella species are natural pathogens of protozoa and can colonise any artificial aquatic environment including cooling towers, air conditioning units, spa pools and bagged soil. Legionella species become a public health risk when the bacteria are aerosolised and subsequently inhaled. There is potential for Legionella to disperse widely, especially after colonisation of cooling towers, leading to outbreaks.
Legionella are fastidious gram negative rods which thrive in warmer waters (20oC-45oC) but have been isolated from waters with temperatures ranging from 6oC to 60oC. They are commonly found in stagnant waters associated with biofilms or various amoebal protozoa.
Legionella pneumophila is the most common cause of Legionnaires’ disease with 98% of reported cases in Europe in 2012 being attributed to this species. Of the 16 serogroups of L. pneumophila, serogroup 1 (SG1) is responsible for most cases of legionnaires disease, 83% of culture positive cases in Europe in 2013 being caused by this serogroup.1 In addition, there are over 50 species of Legionella, of which more than 20 have been implicated in human disease.
In Scotland, there are about 20-40 cases of Legionnaires’ disease a year and around half are travel-associated. Older males are at increased risk of disease and smoking and underlying respiratory disease are risk factors.
1.2 Legionellosis surveillance in Scotland
Enhanced surveillance of Legionella infections has been undertaken by Health Protection Scotland (HPS) in conjunction with the Scottish Haemophilus Legionella Meningococcus Pneumococcus Reference Laboratory (SHLMPRL) since 1994. The purpose of this surveillance is to characterise the Legionella species causing illness; identify the likely source of infection; and inform measures to reduce the public health risk. This involves characterising, identifying and monitoring trends. Surveillance in Scotland is integrated with that of the rest of the UK and with Europe.
Most Legionnaires’ disease cases are hospitalised and the disease is normally detected by urinary antigen diagnostic tests conducted in the hospital microbiology department. The detection of Pontiac fever cases is rare and is mostly identified during outbreaks where serology is the main method of diagnosis, this being performed solely by the reference laboratory. When a Legionnaires’ disease case is confirmed the health protection team from the resident NHS board will undertake an investigation to define risks of exposure and will instigate control measures to prevent others from being exposed. The NHS board is then requested to complete and send an enhanced surveillance form to HPS. This form collects demographic data, information on the clinical presentation and risk factors for each patient; and detailed information on travel away from home during the incubation period of the illness (2-10 days prior to onset of symptoms). All travel-related cases with dates of travel 2-10 days before date of onset are immediately reported to the European Legionnaires’ Disease Surveillance Network (ELDSNet), which aims to quickly identify clusters of cases across Europe and prompt source identification.
HPS publishes summaries every two years of legionellosis in Scotland. Readers are referred to previous reports for more detailed information about past years.2 This report provides an update on cases of legionellosis in Scotland between January 2013 and December 2014.
Under Scottish Government / Health Protection Network guidance on the Management of Public Health Incidents,3 NHS boards should notify HPS of the occurrence of actual or potential Legionnaires’ disease cases. Management of outbreaks affecting more than one NHS board is co-ordinated by HPS. This report provides a summary of sporadic cases and potential incidents, outbreaks and clusters reported to HPS in the period 2013-2014.
1.3 Legionnaires’ disease surveillance in Europe
Only the most severe form of legionellosis, Legionnaires’ disease, is monitored at a European level. This is administered by the European Centre for Disease Control (ECDC), through the European Legionnaires’ Disease Surveillance Network (ELDSNet).4,5
Legionnaires’ disease is monitored in two ways:
- annual submission of datasets of all Legionnaires’ disease cases in member states;1,6
- immediate reporting of travel-related cases of Legionnaires’ disease as they are diagnosed by member states.7 This aims to improve knowledge and information on the epidemiological and microbiological (both clinical and environmental) aspects of Legionnaires’ disease, to locate sources of infection and to prevent further cases of infection.
In addition, ECDC member states are required to notify ECDC of outbreaks or other significant events which may present a risk to European citizens travelling to that country.
ECDC provides case definitions for Legionnaires’ disease, which all member states use. In local outbreaks these definitions may be modified to be more inclusive, to allow more rapid identification of the infection source. For the purposes of routine surveillance and reporting to ECDC, HPS and SHLMPRL use the following definitions (taken from ECDC).8
A confirmed case of Legionnaires’ disease must have clinically defined pneumonia and at least one of the following three laboratory criteria:
- isolation of Legionella species from respiratory secretions or any normally sterile site;
- detection of Legionella pneumophila antigen in urine;
- significant (at least four-fold) rise in specific antibody level to Legionella pneumophila serogroup 1 in paired serum samples.
Probable cases of Legionnaires’ disease must have clinically defined pneumonia and at least one of the following laboratory criteria:
- detection of Legionella pneumophila antigen in respiratory secretions or lung tissue e.g by DFA staining using monoclonal-antibody derived reagents;
- detection of Legionella species nucleic acid in respiratory secretions, lung tissue or any normally sterile site;
- significant (at least four-fold) rise in specific antibody level to Legionella pneumophila other than serogroup 1 or other Legionella species in paired serum samples;
- single high level of specific antibody to Legionella pneumophila serogroup 1 in serum.
Cases are linked epidemiologically if at least one of the following criteria is met:
- environmental exposure;
- exposure to the same common source.
The case definition detailed above is the latest version available on the ELDSNet web pages, taken from the Commission Decision of 8 August 2012, when ECDC case definitions were reviewed and revised.8 These definitions are in line with the recently revised Health Protection Network guidelines which HPS and SHLMPRL use for normal surveillance activities.9
2. Descriptive epidemiology
2.1 Characteristics of cases
The trend of the annual number of reference laboratory diagnosed Legionnaires’ disease cases is shown in figure 1. In 2013, there were 48 cases of which 42 were confirmed and six were probable according to ECDC case definitions shown above. In 2014, there were 30 confirmed cases and four probable cases. All 2013 and 2014 reported cases were Scottish residents.
In 2013, there were two cases of Legionnaires’ disease in Scottish residents exposed, diagnosed and treated overseas. These cases will not be included in this report. In 2014, a case description for one case could not be determined and was classified as unconfirmed. This case is excluded from this report.
Incidence of Legionnaires’ disease in 2013 and 2014 was nine cases per million population and 6.5 cases per million respectively. These rates are a decline from 19.6 cases per million in 2012 in which a large Legionnaires’ disease outbreak occurred in Edinburgh and are consistent with rates in previous years in Scotland (six cases per million in 2011, 3.4 in 2010 and 4.8 in 2009). The incidence rates for Scotland in 2013 and 2014 are also lower than the 2013 European incidence rate of 11.4 cases per million.1
Cases of Legionnaires’ disease were diagnosed in every quarter of 2013 and 2014. The highest number of cases was seen in quarter three (July to September) for both years (Figure 2). This is similar to Europe observations, with the number of travel cases reported increasing in the summer months.1,6 The large number of cases reported in quarter 3 of 2013 is related to:
- the Legionnaires’ disease outbreak in NHS Greater Glasgow and Clyde;
- the small cluster in Ayrshire and Arran;
- the national cluster of L. longbeachae.
Table 1 shows the percentage of male cases in Scotland from 2000 to 2014. In 2013, 60% of cases were male while in 2014 62% were. This pattern has previously been observed in Scotland and elsewhere: on average there are twice as many male cases as female cases. In 2013 in Europe, the percentage of male cases was 58.3%.1
The majority of Legionnaires’ disease cases between 2000 and 2014 were aged 40 years or older (Figure 3). In 2013, 98% of cases were 40 or older and all cases in 2014 were 40 or older. Over half of the cases in 2013 were between 50 and 69 years old (27 cases, 56%) while in 2014, the majority of cases were between 60 and 79 years old (23 cases, 65%). Overall, for 2013 and 2014, the most common age ranges of cases were 60-69 and 70-79 years with 24 cases within each age range accounting for 59% of cases reported in these years.
2.5 Risk factors
Both tobacco smoking and respiratory disease are known risk factors for Legionnaires’ disease. In 2013 and 2014, 45% of cases were smokers, 50% did not smoke, and smoking status was unknown for 5% of cases. The proportion of smokers is smaller than in previous years where 61% were smokers in 2011-2012 (31% non-smokers and 8% unknown) and 54% were in 2009-2010 (27% non-smokers and 19% unknown) respectively.
Being immunocompromised is a risk factor for Legionnaires’ disease as with many other pathogens. In 2013 and 2014, 11% of cases were immunocompromised while 78% were not immunocompromised and immune status was unknown or not recorded for 11% of cases. This is compared with 29% being immunocompromised in 2011-2012 (64% not immunocompromised and 7% unknown or not recorded) and 20% in 2009-2010 (75% not immunocompromised and 5% unknown or not recorded.
2.6 Clinical presentation
Data presented in this report describe cases of Legionnaires’ disease in 2013 and 2014. No Pontiac fever cases were reported to HPS during this period.
In 2013, 92% of Legionnaires’ disease cases presented with pneumonia, and in 2014, all cases presented with pneumonia. Clinical symptoms include (in no particular order) fever, shortness of breath, dry cough, headache, muscle pain, lethargy, confusion, nausea, vomiting, diarrhoea, dizziness, shivers, thoracic pain, pleuritic pain, chest pain and collapse.
In 2013 there were two recorded deaths from Legionnaires’ disease and four in 2014 (Table 2). Such mortality data do not necessarily reflect the recorded cause of death on patient death certificates.
Case fatality rates in 2013 and 2014 are 4% and 12% respectively. This resulted in a mean case fatality rate of 7% in the two-year period. This is consistent with previous two-yearly mean case fatality rates in Scotland (8.8% in 2011-2012; 7.3% in 2009-2010; 10.3% in 2007-2008). Scotland’s case fatality rate still remains lower than the average European rate which was 10% in 2012 and 2013.1,6 Given the small annual number of deaths in Scotland, case fatality rates are subject to large variation and are therefore difficult to interpret.
3. Suspected settings for Legionella exposure
Of the 82 Legionnaires’ disease cases reported to HPS in 2013 and 2014, 46% were community-acquired, 54% were travel-associated and none were hospital-acquired. This distribution is shown in table 3 and shows a decrease in community-acquired disease when compared to the previous two years which was high due to the large 2012 south-west Edinburgh outbreak (73% community-acquired; 25% travel-related; 1% hospital-acquired).
3.1 Travel-associated cases
Table 4 shows the travel destinations of each travel-related case according to continent and European country visited. In 2013 and 2014, stays in accommodation in Europe were associated with the majority of travel-related cases, with common destinations of Scottish travellers (e.g. the UK, Spain, Turkey, Greece and Italy) being implicated in most travel-related cases. Some cases visited more than one destination and this is reflected in the numbers in Table 4.
In 2013, 16 cases were reported to ELDSNet of which eight cases were linked with seven different clusters, while in 2014, 24 cases were reported to ELDSNet and one case was associated with a cluster. A cluster is defined by ELDSNet as when cases from different countries are suspected as having contracted Legionnaires’ disease from the same accommodation site in a two-year period.
3.2 Community-acquired cases
Overall, between 2013 and 2014 there were 38 community-acquired cases of Legionnaires’ disease.
The source of Legionella is rarely identified in sporadic, community cases due to its ubiquitous environmental distribution.
4. Cases of Legionnaires’ disease in travellers to Scotland
In 2013, ELDSNet received a report of a case of Legionnaires’ disease in a traveller to Scotland which was linked to the Greater Glasgow and Clyde cluster. In 2014, a case of Legionnaires’ disease in a traveller to the UK was hospitalised in Scotland. Due to the extensive travel history of the case, the source of the infection could not be determined.
5. Outbreaks and clusters
There were three actual or potential Legionnaires’ disease outbreaks during the 2013-2014 period, all occurring in 2013:
- 12 cases of Legionnaires’ disease in NHS Greater Glasgow and Clyde;
- three cases of Legionnaires’ disease in North Ayrshire;
- cases of Legionella longbeachae throughout Scotland.
5.1 NHS Greater Glasgow and Clyde outbreak
Between the beginning of June 2013 and the end of July 2013, NHS Greater Glasgow and Clyde led an investigation into 12 Legionnaires’ disease cases. All cases were linked to a distinct area either through residence, work or social links. There were three or possibly four distinct temporal clusters which supports the scenario of an intermittent emission of Legionella from a single source; the nature of which could not be identified. Cooling towers in the area were chlorine ‘shock dosed’; however, cases continued to be reported and this, paired with the fact most cases could be linked to a geographically distinct area, supported a smaller localised dispersal. The weather was exceptionally warm during this period which would have encouraged both Legionella growth and residents spending more time outdoors, increasing the likelihood of exposure to Legionella contaminated aerosols.
5.2 Cluster of Legionnaires’ disease in NHS Ayrshire and Arran
In September, NHS Ayrshire and Arran, working with colleagues in Environmental Health, HPS and the Health and Safety Executive, led an investigation into a small cluster of Legionnaires’ disease in residents of North Ayrshire. No common source was identified.
5.3 Cluster of Legionnaires’ disease caused by Legionella longbeachae throughout Scotland
An investigation into a cluster of of six confirmed cases and one probable case of Legionnaires’ disease caused by L. longbeachae was undertaken by HPS, NHS Lothian and NHS Tayside between August and September of 2013.10 All cases had previous exposure to compost within the incubation period and were keen gardeners. Typing of L. longbeachae in patient samples and in potting soils purchased by some cases, where available, was undertaken and similarity was found between and within clinical and environmental isolates. No link was established regarding the origin and manufacturing of the different composts sampled.
6. SHLMPRL testing for Legionella in 2013 and 2014
Overall, 4611 samples were received by SHLMPRL for testing in 2013, a 6% decrease on the number received in 2012 when a large outbreak was experienced in Edinburgh. In 2014, 4382 samples were received, a decrease of 5% on 2013 (Table 5). The increase in samples received from NHS Greater Glasgow and Clyde and NHS Ayrshire and Arran in 2013 is related to the outbreak of Legionnaires’ disease in Greater Glasgow and Clyde and the investigation of the cluster in Ayrshire and Arran. During this period, there was increased awareness of Legionnaires’ disease and case finding was encouraged. The large percentage change in the number of samples received from NHS Orkney is due to the small population size of the board.
6.1 Characteristics of laboratory confirmed cases of Legionella
In 2013 and 2014, 54 (50%) of all positive samples were diagnosed by urinary antigen test (which can only confirm L. pneumophila serogroup 1), 16 (15%) by PCR, seven (7%) by single high titre, 12 (11%) by sero-conversion and 18 (17%) by culture (Table 6).
A total of 18 samples were confirmed by culture from patients in 2013 and 2014. Of these, eight were L. pneumophila, nine were L. longbeachae and one was L. maceachernii. The L. pneumophila Sg 1 isolates by monoclonal subtype were Philadelphia (three), Knoxville (three) and Benidorm (two).
Sequence based typing was performed on four of the L. pneumophila isolates. This technique sequences seven genes allowing a genotype profile to be created which is invaluable for tracing outbreaks’ environmental source, where one can be identified.
6.2 Environmental samples
Overall, 66 environmental samples were sent for testing in 2013 and 90 in 2014. This is compared to 48, 83, 168, 252, 90 and 183 in 2012, 2011, 2010, 2009, 2008 and 2007 respectively. The species, serotypes and subtypes are presented in Table 7.
The most commonly isolated species was Legionella anisa with 41 out of 156 (26%) environmental samples positive for this species. This is followed by L. pneumophila Sg 1 with 35 out of 156 (22%) samples positive, L. pneumophila Sg 6 with 23 out of 156 (15%) and L. longbeachae with 17 out of 156 (11%). The most commonly isolated subtypes of L. pneumophila Sg 1 in environmental samples were OLDA, Bellingham and Knoxville with 20 (57%), 5 (14%) and 4 (11%) out of 35 samples positive for L. pneumophila Sg 1 respectively. The remaining species isolated from environmental samples were L. erythra and L. feelei with 4 (3%) and 3 (2%) positive respectively.
SHLMPRL encourages labs to send all Legionella samples for confirmation as mip gene sequencing identifies all Legionella species.
6.3 Laboratory investigations
6.3.1 NHS Greater Glasgow and Clyde outbreak
All of the 12 confirmed cases in this outbreak were primarily diagnosed using the Legionella urinary antigen assay, nine at local laboratories and three at the reference laboratory. Samples referred to SHLMPRL were confirmed by enzyme immunoassay (EIA). Serology was also undertaken by SHLMPRL on ten cases and molecular typing was performed on two isolates from cases. Genetic sequence based typing (SBT) showed both isolates were L. pneumophila Sg 1 Philadelphia ST 37 and were indistinguishable.
6.3.2 Cluster of Legionnaires’ disease in NHS Ayrshire and Arran
In order to ensure confidentiality for the small number of cases in this cluster, details of the laboratory investigation for these three cases are not reported here.
6.3.3 National cluster of Legionnaires’ disease caused by Legionella longbeachae
All cases in this outbreak were tested using the urinary antigen assay but were negative as the assay can only detect L. pneumophila Sg1 antigens in urine. For the cases notified in NHS Lothian, all were diagnosed through PCR and cultures were also taken. Confirmation of positive samples was undertaken by SHLMPRL including serological testing. For the cases diagnosed in NHS Tayside, specimens from patients were cultured for a broad range of bacteria and positive samples were sent to SHLMPRL for characterisation and PCR was positive on one sample and culture positive in all cases. Where tested, all cases showed serological evidence of infection with L. longbeachae.
7. New and planned developments over the next two years
7.1 Further understanding of Legionnaires’ disease caused by non-pneumophila species
Work is underway within Health Protection Scotland to increase understanding of Legionnaires’ disease caused by non-pneumophila species through the use of data linkage. By linking to hospital admissions, Scottish Index of Multiple Deprivation (SIMD) and prescribing data, HPS aims to increase understanding of the short-term and long-term clinical outcomes of patients infected with non-pneumophila species. Comparisons with patients infected with L. pneumophila will also be undertaken.
7.2 Understanding the role of the environment in L. longbeachae transmission
The University of Strathclyde, in collaboration with HPS, has applied for a grant from the National Environment Research Council (NERC). The aim of the intended research is to further understand the role of the environment in the transmission of L. longbeachae through the sampling of bioaerosols in composting sites and growing media production facilities to determine what Legionella and amoeba species are present. Work will also be undertaken to further characterise the relationship between amoebae and L. longbeachae and comparisons will be made with L. pneumophila. Additionally, sampling procedures for the culture of bioaerosols and compost components will be evaluated.
The authors would like to thank the microbiologists, staff of SHLMPRL, consultants in public health medicine, clinicians, nurses, public health teams and other staff who assist in the submission of samples to SHLMPRL and in the completion of surveillance forms. Their assistance and dedication underpins a better understanding of the national epidemiological picture.
- European Centre for Disease Prevention and Control. Legionnaires’ disease in Europe in 2013. Available from: http://ecdc.europa.eu/en/publications/_layouts/forms/Publication_DispForm.aspx?List=4f55ad51-4aed-4d32-b960-af70113dbb90&ID=1288. (accessed 29 August 2015).
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- Health Protection Network. Guideline on the management of Legionella incidents, outbreaks and clusters in the community. Available from: http://www.hps.scot.nhs.uk/resp/guidelinedetail.aspx?id=61062&subjectid=185,97. (accessed 29 August 2015).
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