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Respiratory Infections

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29 August 2017

Legionellosis in Scotland 2015-2016

Introduction

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 sp. become a public health risk when the bacteria become aerosolised and subsequently inhaled. There is potential for Legionella to become dispersed widely, especially after colonisation of cooling towers, leading to outbreaks.

Legionella are fastidious Gram negative rods which thrive in warmer waters (15°C-46°C) but have been isolated from waters with temperatures ranging from 6°C to 60°. They are commonly found in stagnant waters associated with biofilms or within various protozoa.

Legionella pneumophila is the most common cause of Legionnaires’ disease with 96.1% of reported culture-confirmed cases in Europe in 2015 being attributed to this species. Of the 16 serogroups of L. pneumophila, serogroup 1 (Sg1) is responsible for most cases of Legionnaires’ disease; 85.6% of culture positive cases in Europe in 2015 were caused by this serogroup.1 In addition, there are a further 61 species of Legionella, of which more than 20 have been implicated in human disease.

In Scotland, about 20-40 cases of Legionnaires’ disease are reported every year, which are mostly travel associated. Older males are at increased risk of disease and smoking and underlying respiratory disease are risk factors.

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 enhanced 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 detected by diagnostic tests usually conducted in the hospital (Table 5). The detection of Pontiac fever cases is rare and mostly occurs during outbreaks when awareness of legionellosis is high among healthcare staff. Patient samples are tested locally but are usually confirmed by the reference laboratory.2 When the case is confirmed, the health protection team from the resident NHS board will carry out an investigation which aims to define any risks for exposure and to instigate any 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 (2-14 days prior to onset of symptoms in Scotland). All cases that are travel-related with date 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.3 This report provides an update on cases of legionellosis in Scotland between January 2015 and December 2016.

Under Scottish Government / Scottish Health Protection Network guidance,4 NHS boards should notify HPS of the occurrence of actual or potential Legionnaires’ disease cases. Management of outbreaks which affect more than one NHS board is co-ordinated by HPS. This report provides a summary of sporadic cases and those outbreaks reported to HPS in the period 2015-2016.

Legionnaires’ disease surveillance in Europe

Only the severe form of legionellosis, Legionnaires’ disease, is monitored at a European level. This monitoring is administered by the European Centre for Disease Control (ECDC), through the European Legionnaires’ Disease Surveillance Network (ELDSNet).5, 6

Legionnaires’ disease is monitored in two ways:

  1. annual submission of datasets of all Legionnaires’ disease cases in member states;1
  2. 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 for the purposes of reporting to ECDC. In local outbreaks these definitions may be modified to be more inclusive, to allow more rapid identification of the infection source.

The following case definitions were used during 2015 and 2016 and are taken from ECDC.7

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

All Legionnaires’ disease cases presented in this report were defined according to the current ECDC definitions.

Descriptive epidemiology

Characteristics of cases

The trend of the annual number of reference laboratory diagnosed Legionnaires’ disease cases is shown in Figure 1. In 2015 there were 39 cases of which 33 were confirmed and six were probable cases according to ECDC case definitions. In 2016 there were 34 cases of which 31 were confirmed and three were probable cases. In 2015, one case was a resident of Latvia; in 2016, one case was a resident of Spain and another resident of the United States of America.

Incidence

Incidence of Legionnaires’ disease in 2015 and 2016 was 7.3 cases per million population and 6.3 cases per million, respectively. These rates are consistent with the incidence of 6.4 per million population in 2014 and a decline from the 9.0 cases per million in 2013 and 19.6 in 2012 in which there was a large Legionnaires’ disease outbreak in Edinburgh. The incidence rates for Scotland in 2015 and 2016 are also lower than the 2015 European incidence rate of 13.6 cases per million.1

Cases of Legionnaires’ disease were diagnosed in every quarter of 2015 and 2016. The highest number of cases was seen in quarter three (July to September) for both years (Figure 2). This is similar to what is observed in Europe with the number of travel cases reported increasing in the summer months.1

Gender

Table 1 shows the percentage of male cases in Scotland from 2000 to 2016. In 2015, 64.1% of cases were male while 70.6% were male in 2016. This pattern has previously been observed in Scotland and elsewhere with on average there are twice as many male cases as female cases. In 2015 in Europe, the percentage of male cases was 71.3%.1

Age

The majority of Legionnaires’ disease cases between 2000 and 2016 are aged 40 years or older (Figure 3). 97% and 94% of cases were 40 or older in 2015 and 2016, respectively. The majority of cases in 2015 were between 50 and 69 years old (25 cases, 64%) while, in 2016, the 60-69 age group had the highest number of cases (12 cases, 35%) with eight cases each in the 50-59 and 70-79 age groups. Overall, for 2015 and 2016 the most common age range of cases was 60-69 years with 26 cases accounting for 36% of cases reported in these years.

Risk factors

Both tobacco smoking and respiratory disease are known risk factors for Legionnaires’ disease. In 2015 and 2016, 51% of cases were smokers, 31% did not smoke and smoking status was unknown for 18% of cases. The proportion of smokers is higher than in 2013-2014 when 45% of cases were smokers (50% non-smokers and 5% unknown) and lower than in 2011-2012 when 61% were smokers (31% non-smokers and 8% unknown).

Being immunocompromised is a risk factor for Legionnaires’ disease as with many other pathogens. In 2015 and 2016, 18% of cases were immunocompromised either through immunosuppression with steroids or through an underlying condition, while 82% were not immunocompromised and immune status was unknown or not recorded for 2% of cases. This is compared with 11% (78% not immunocompromised and 11% unknown or not recorded) and 29% (64% not immunocompromised and 7% unknown or not recorded) of individuals being immunocompromised in 2013-2014 and 2011-2012, respectively.

Having underlying co-morbidities is also a risk factor for Legionnaires’ disease. Of the 73 cases reported to HPS in 2015 and 2016, 51 (70%) cases had an underlying co-morbidity. These co-morbidities were varied and the most common include cardiovascular disease, chronic lung disease, diabetes and cancer.

Clinical presentation

Data presented in this report describe cases of Legionnaires’ disease in 2015 and 2016. Two Pontiac fever cases were reported to HPS during this period and are not included in this report.

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.

Mortality

In 2015 there were two recorded deaths from Legionnaires’ disease and four in 2016 (Table 2). Such mortality data do not necessarily reflect the cause of death recorded on patient death certificates.

Case fatality rates in 2015 and 2016 were 5% and 12%, respectively. This resulted in a mean case fatality rate of 8.2% in the two-year period. This is consistent with previous two-yearly mean case fatality rates in Scotland (7.3% in 2013-2014, 8.8% in 2011-2012; 7.3% in 2009-2010; 10.3% in 2007-2008). Scotland’s case fatality rate is also consistent with the European rate which was 8.1% in 2015.1 The small number of annual deaths in Scotland makes case fatality rates subject to large variation and therefore difficult to interpret.

Suspected settings for Legionella exposure

Of the 73 Legionnaires’ disease cases reported to HPS in 2015 and 2016, 30.1% were considered to be community-acquired, 68.5% were travel-associated, and 1.4% had an exposure that was undetermined. There were no cases of nosocomially-acquired legionellosis. This distribution is shown in Table 3 and is consistent with previous years in which there has not been a community cluster or outbreak.

Travel-associated cases

Table 4 shows the travel destinations of each travel-related case according to continent and European country visited. In 2015 and 2016, stays in accommodation in Europe were associated with the majority of travel-related cases with destinations such as Spain, Italy, Greece and Turkey being implicated in most. Some cases visited more than one destination (Table 4).

The number of cases of travel-related Legionnaires’ disease who had stayed in accommodation in Asia has increased since 2014, which may be a reflection of increased travel to this area. It should also be noted that in the latter part of 2016 an increase in cases of Legionnaires’ disease in travellers returning from Dubai occurred and some Scottish cases were associated with this increase.9,10

In 2015, 22 cases were reported to ELDSNet of which nine were linked with eight different clusters, and in 2016, 19 cases were reported to ELDSNet of which eight were linked with seven clusters. A cluster is defined by ELDSNet as when cases from the same or different countries are suspected as having contracted Legionnaires’ disease from the same accommodation site in a two-year period.

Community-acquired cases

Overall, from 2015 to 2016 there were 22 community-acquired cases of Legionnaires’ disease. All cases were sporadic and no community clusters of Legionnaires’ disease occurred in 2015-16.

The source of Legionella is rarely identified in sporadic, community cases due to its ubiquitous environmental distribution.

Cases of Legionnaires’ disease in travellers to Scotland

In 2016, ELDSNet received three reports of cases of Legionnaires’ disease in travellers to Scotland. All accommodation sites in which the cases stayed were risk assessed and appropriate measures were in place.

Outbreaks

There were no clusters or outbreaks of Legionnaires’ disease in 2015 and 2016 in Scotland.

SHLMPRL testing for Legionella in 2015 and 2016

Overall, 4433 samples were received by SHLMPRL for testing in 2015 and represents a 1% increase on the number received in 2014. In 2016, 4578 samples were received, an increase of 3% on 2015 (Table 5). As there was no Legionnaires’ disease clusters or outbreaks in Scotland the increase in testing may be related to an increase in returning travellers presenting with respiratory symptoms. Awareness of the increase of Legionnaires’ disease cases in returning travellers from Dubai may have led to increased testing due to a number of alerts from ECDC.

Large fluctuations in testing are likely to be related to the small population size of some NHS boards.

As always, SHLMPRL would encourage all laboratories to send any positive samples for confirmation.

Characteristics of laboratory confirmed cases of Legionella

In 2015 and 2016, of 100 positive samples, 56 (56%) were diagnosed by urinary antigen test (which can only detect L. pneumophila serogroup 1), 21 (21%) by PCR, 16 (16%) by culture, six (6%) by single high titre and one (1%) by seroconversion (Table 6).

A total of 16 samples were confirmed by culture from patients in 2015 and 2016. Of these, 12 were L. pneumophila, one was L. longbeachae, one was L. macaechernii, one was L. bozemanii and the other L. micdadei. The L. pneumophila Sg 1 isolates identified by monoclonal subtype were Philadelphia (four), Allentown/France (two), Benidorm (two) and Bellingham (one).

Sequence-based typing was performed on eight of the L. pneumophila isolates. This technique sequences seven genes allowing a genotype profile to be created which is invaluable in outbreaks and can facilitate tracing of environmental sources.

Environmental samples

Overall, 18 environmental samples were received for testing in 2015 and 35 in 2016. This is a decrease compared to 53, 90, 48, 83, 168 and 252 in 2014, 2013, 2012, 2011, 2010 and 2009, respectively. The decrease is likely related to no clusters or outbreaks occurring in 2015 and 2016 and therefore sampling of environmental sources was not undertaken on a large scale. The species, serotypes and subtypes are presented in table 7.

The most commonly isolated species was L. pneumophila Sg 4 Portland with 18 out of 53 (34%) environmental samples positive for this species. This is followed by L. anisa with five out of 53 (9%) samples positive, L. pneumophila Sg 6, L. pneumophila Sg 7 and L. taurinensis with four samples positive each (8% each) and L. pneumophila Sg 2 with three samples positive (6%). Of the four L. pneumophila Sg 1 positive samples, two were Heysham (50%), one was Olda (25%) and the other Knoxville (25%). The remaining species isolated from environmental samples were L. longbeachae (two, 4%), L. sainthelensi (two, 4%), L. nautarum (one, 2%) and L. dumoffii (one, 2%).

SHLMPRL encourages all labs to send Legionella species for confirmation as sequence-based typing identifies all Legionella species.

New and planned developments over the next two years

Update of Guideline on Management of Legionella Incidents, Outbreaks and Clusters in the Community

A planned update of the Guideline on Management of Legionella Incidents, Outbreaks and Clusters in the Community11 is underway and should be completed by the end of 2017. The update will consist of the inclusion of the new case definitions and guidance around the testing of household water supplies during the investigation of sporadic cases and clusters of Legionnaires’ disease.

From 2017, the Scottish case definition for Legionnaires’ disease have been modified to be in line with the Public Health England (PHE) case definitions with the main change being the addition of PCR positive cases being considered confirmed. These modified case definitions are detailed below:

A confirmed case of Legionnaires’ disease must have clinically defined pneumonia and at least one of the following four laboratory criteria:

  • isolation of Legionella from respiratory secretions or any normally sterile site;
  • detection of Legionella pneumophila antigen in urine;
  • detection of Legionella spp. nucleic acid (e.g. by PCR) in a lower respiratory tract specimen (e.g. sputum or bronchoalveolar lavage (BAL));
  • 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;
  • 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.

Whole genome sequencing of human and environmental Legionella isolates in Scotland

The Chief Scientist Office for Scotland is funding a study titled ‘Genomic epidemiology of Legionnaires’ disease in Scotland: towards effective outbreak investigation’. The lead investigator is Professor Ross Fitzgerald, The Roslin Institute, Edinburgh in collaboration with the Scottish Reference laboratory and others. The project makes use of whole genome sequencing technology on clinical and environmental Legionella isolates spanning 30 years to provide the highest level of genotypic resolution. To date the project has sequenced over 400 Scottish Legionella isolates (Bryan Wee, Project Postdoctoral scientist) which will be studied in the context of the wider global diversity of genomic data already available. The study will uncover the diversity of genetic subtypes of clinically relevant Legionella in Scotland to inform investigations into source attribution in complex outbreaks. In addition, the project will also examine the potential of using culture-independent metagenomic sequencing to probe the diversity of Legionella spp. in environmental and patient samples.

Acknowledgments

The authors would like to thank the microbiologists, 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.

References

  1. European Centre for Disease Prevention and Control (ECDC). Legionnaires’ disease in Europe in 2015. 2017. Available from: https://ecdc.europa.eu/en/publications-data/legionnaires-disease-europe-2015. (accessed 25 August 2017).
  2. NHS Greater Glasgow and Clyde. Scottish Haemophilus, Legionella, Meningococcus & Pneumococcus Reference Laboratory. Available from: http://www.nhsggc.org.uk/about-us/professional-support-sites/microbiology/scottish-microbiology-reference-laboratories/scottish-haemophilus-legionella-meningococcus-pneumococcus-reference-laboratory/. (accessed 25 August 2017).
  3. Health Protection Scotland (HPS). Legionella. Available from: http://www.hps.scot.nhs.uk/resp/legionella.aspx?subjectid=185,97. (accessed 25 August 2017).
  4. Scottish Government. Management of public health incidents: guidance on the roles and responsibilities of NHS led incident management teams (Scottish Health Protection Network Scottish Guidance 12 (2017 edition)). 2017. Available from: http://www.hps.scot.nhs.uk/pubs/detail.aspx?id=1266. (accessed 25 August 2017).
  5. ECDC. Legionnaires’ disease. Available from: https://ecdc.europa.eu/en/legionnaires-disease. (accessed 25 August 2017).
  6. ECDC. European Legionnaires’ Disease Surveillance Network (ELDSNet). Available from: https://ecdc.europa.eu/en/about-us/partnerships-and-networks/disease-and-laboratory-networks/eldsnet. (accessed 25 August 2017).
  7. Beauté J, Zucs P, de Jong B. Risk for travel-associated Legionnaires’ disease in Europe, 2009. Emerging Infectious Diseases, 2012;18(11):1811-16. Available from: https://wwwnc.cdc.gov/eid/article/18/11/12-0496_article. (accessed 25 August 2017).
  8. ECDC. Legionnaires’ disease outbreak case definitions. Available from: https://legionnaires.ecdc.europa.eu/?pid=202. (accessed 25 August 2017).
  9. ECDC. Increase of cases of Legionnaires’ disease in EU travellers returning from Dubai, October-December 2016 (risk assessment). Available from: https://ecdc.europa.eu/en/publications-data/increase-cases-legionnaires-disease-eu-travellers-returning-dubai-october. (accessed 25 August 2017).
  10. ECDC. Epidemiological update: Legionnaires’ disease cases associated with travel to Dubai, 22 June 2017. Available from: https://ecdc.europa.eu/en/news-events/epidemiological-update-legionella-dubai-22-june-2017. (accessed 25 August 2017).
  11. Health Protection Network. Guideline on the management of Legionella cases, incidents, outbreaks and clusters in the community. Health Protection Network Scottish Guidance 2 (2014 Edition). 2014. Available from: http://www.hps.scot.nhs.uk/resp/resourcedetail.aspx?id=200. (accessed 25 August 2017).
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