Cluster of Legionella longbeachae cases in Scotland in September/October Report from a national Incident Management Team

Transcription

1 Cluster of Legionella longbeachae cases in Scotland in September/October 2013 Report from a national Incident Management Team Published June 2014

2 Acknowledgements The collaboration of those involved in this investigation is gratefully acknowledged. This includes Health Protection Teams, Environmental Health Teams, microbiologists, public analysts, the Growing Media Association and Horticultural Trades Association. Health Protection Scotland is a division of NHS National Services Scotland. Health Protection Scotland website: Published by Health Protection Scotland, NHS National Services Scotland, Meridian Court, 5 Cadogan Street, Glasgow G2 6QE. First published June 2014 Health Protection Scotland 2014 Reference this document as: Health Protection Scotland. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 Health Protection Scotland, 2014 [Report] Contributing Authors: Alison Potts on behalf of the IMT Health Protection Scotland has made every effort to trace holders of copyright in original material and to seek permission for its use in this document. Should copyrighted material have been inadvertently used without appropriate attribution or permission, the copyright holders are asked to contact Health Protection Scotland so that suitable acknowledgement can be made at the first opportunity. Health Protection Scotland consents to the photocopying of this document for professional use. All other proposals for reproduction of large extracts should be addressed to: Health Protection Scotland NHS National Services Scotland Meridian Court 5 Cadogan Street Glasgow G2 6QE Tel: +44 (0) NSS.HPSEnquiries@nhs.net Designed and typeset by: Graphics Team, Health Protection Scotland

3 Table of Contents Abbreviations -ii 1. Introduction 1 2. Background Legionella bacteria and legionellosis Legionnaires disease in Scotland Legionnaires disease caused by L. longbeachae 2 3. Investigation Timeline Epidemiological investigation Clinical microbiological investigation Environmental investigation Environmental microbiology investigation AFLP typing Whole genome sequencing Risk management Prevention of further exposure to hazardous agent Care of cases Risk communication Communication with clinicians Communication with the public Communication with retailers Communication with manufacturers Discussion and conclusion Discussion Conclusion 22 7.Lessons learned and recommendations Lessons learned Recommendations References Appendices Members of the national IMT 27 Cluster of Legionella longbeachae cases in Scotland in September/October 2013 i

4 Abbreviations ECDC ELDSNet ESS GMA HPN HPS HPT HTA IMT ICU NHS NHS NSS PAG PCR PHE PHNI PHW European Centre for Disease Prevention and Control European Legionnaires Disease Surveillance Network City of Edinburgh Council Scientific Services Growing Media Association Health Protection Network Health Protection Scotland Health Protection Team Horticultural Trades Association Incident Management Team Intensive Care Unit National Health Service NHS National Services Scotland Problem Assessment Group Polymerase Chain Reaction Public Health England Public Health Northern Ireland Public Health Wales Sg1 Serogroup 1 SHLMPRL TSS WGS Scottish Haemophilus, Legionella, Meningococcus, Pneumococcus Reference Laboratory Dundee City Council Tayside Scientific Services Whole Genome Sequencing ii Cluster of Legionella longbeachae cases in Scotland in September/October 2013

5 1. Introduction In the period August to September 2013, six confirmed and one probable case of Legionnaires disease caused by L. longbeachae were reported in NHS Lothian and NHS Tayside. The six confirmed cases were severely unwell and all required treatment in intensive care units, including ventilation. All cases survived. The majority of cases were keen gardeners and had exposure to growing media, soils and water in the garden during their incubation period. Prior to this cluster, eleven sporadic cases of Legionnaires disease caused by L. longbeachae infection had been reported to Health Protection Scotland, in the period Given the unprecedented concurrent nature and close geographical proximity of these cases, an investigation was undertaken. Due to cases being identified in two NHS boards, the investigation was co-ordinated by HPS. 1 This report details the investigation undertaken. Members of the national IMT are listed in Appendix 1. This report has been approved by the IMT. Cluster of Legionella longbeachae cases in Scotland in September/October

6 2. Background 2.1 Legionella bacteria and legionellosis Legionella bacteria are ubiquitous and are often isolated from water and soil samples. There are two forms of legionellosis, the illness caused by Legionella bacteria infection: Legionnaires disease (pneumonia characterised by fever, myalgia and cough); and Pontiac fever (a milder flu-like illness without pneumonia). Legionnaires disease is recognised as an important cause of severe, sporadic communityacquired pneumonia. Pontiac fever is rarely reported outside outbreaks and is likely to be under ascertained. Pneumonias caused by Legionella species are not uncommonly associated with respiratory failure and thus have a relatively high mortality rate. 2.2 Legionnaires disease in Scotland The detection of any member of the Legionella genus in a clinical sample by a microbiological laboratory has to be notified to the relevant NHS board and to Health Protection Scotland (HPS) under the Public Health (Scotland) Act of HPS undertakes enhanced surveillance of notified cases of Legionella infections in conjunction with NHS boards and the Scottish Haemophilus, Legionella, Meningococcus and Pneumococcus Reference Laboratory (SHLMPRL). The purpose of enhanced surveillance is to characterise the Legionella species causing infection and identify likely sources and exposures to the organism. Legionnaires disease is monitored by the European Centre for Disease Control (ECDC 3 ) through the European Legionnaires Disease Surveillance Network (ELDSNet 4 ). Guidelines on the management of outbreaks of Legionnaires disease have been developed by the Health Protection Network (HPN). 5 The incidence of Legionnaires disease in Scotland is low. There are usually between 20 and 40 cases per year, the majority of who contract the infection overseas. 6 Older age and male gender are both associated with increased risk, as are smoking and underlying respiratory disease. Cases range in severity from those who can be treated with antibiotics at home and make a full recovery, to those who require invasive ventilation for prolonged periods, to death. The mortality rate in Scotland is around 9%, 7 which is slightly lower than that seen in the whole of Europe (10%). 8 The majority of cases in Scotland are caused by L. pneumophila Serogroup 1 (Sg1). There have been a number of outbreaks of Legionnaires disease in Scotland in the last few years. These include an outbreak associated with cooling towers in the south-west of Edinburgh and an outbreak of 12 cases in a residential area for which no source could be found, despite extensive investigation. In addition there was a significant outbreak of Pontiac fever associated with sports facilities in a hotel. All of these outbreaks were caused by different strains of L. pneumophila Sg Legionnaires disease caused by L. longbeachae L. longbeachae is an uncommon species of Legionella and like L. pneumophila, it can cause a wide range of symptoms from mild flu-like illness to acute atypical community acquired pneumonia and death. The major source of human infection is considered to be commercial growing media (soils and composts which are sold through garden centres and are a blend of some or all of: soil, peat, composted green waste, sand and minerals; used for growing plants) and other composted 2 Cluster of Legionella longbeachae cases in Scotland in September/October 2013

7 materials such as bark and sawdust. Unlike other known strains of Legionella, L. longbeachae has rarely been identified in man-made water systems. 9 Legionnaires disease caused by L. longbeachae may be missed or diagnosed late, as urine tests which are routinely used to identify most cases of Legionnaires disease do not detect L. longbeachae. Confirmed diagnosis of L. longbeachae infection requires culture of the organism from clinical specimens, whereas elevated specific antibody titre and detection by polymerase chain reaction (PCR) may be used to diagnose probable infection. These tests may not be routinely performed or available in routine diagnostic laboratories. The number of cases of Legionnaires disease caused by L. longbeachae in Europe is small but growing. However, in Australia and New Zealand up to half of Legionnaires disease cases are caused by L. longbeachae. Investigations into growing media in Australia have revealed that a large proportion of Australian growing medias are contaminated with Legionella bacteria 10 similar studies in other countries including the UK have corroborated these findings. 11 A main difference between Australian and New Zealand growing media and those produced in Europe is that Australian and New Zealand growing media are made mostly from composted pine sawdust and bark, whereas in Europe growing media are mostly peat based. 9 The proportion of peat and composted material in growing media in the UK is changing to support UK legislation 13 to preserve peat resources. Peat is being replaced with composted green waste. Bags of growing media in Australia and New Zealand are labelled with a warning about risk of exposure to L. longbeachae and advice to wear gloves and a facemask whilst handling the growing media. 12 This labelling is described in industry standards which were introduced in 2003 (Australia) and 2005 (New Zealand). These standards are not statutory but there is widespread compliance. However, it is not clear that introduction of these standards has been effective, as there has been no decline in numbers of cases of Legionnaires disease caused by L. longbeachae, since their introduction. Currently in the UK there is a British Institute of Standards for composted green waste PAS This standard states that: the following information about each consignment of conforming compost dispatched shall be printed on packaging or on a separate document supplied to the compost recipient..h) warning about product misuse, risks when handling and safety advice or symbols as appropriate; The Association for Organics Recycling recommends in their guidance on L. longbeachae 16 that to meet the PAS 100 standard, a warning statement should be included in labelling which reads: SAFE HANDLING AND USE Every effort has been made to ensure this compost contains no germs, sharp fragments, toxins or regenerative plant parts. However the compost producer cannot guarantee they will never be present. As with all products of this type, wear gloves when handling and wash hands after use. During handling avoid inhaling any dust or water vapour or droplets from it, or ingesting any of it Information from previous discussions with the horticultural industry suggests that general wording on a label may exacerbate liability issues and that a voluntary agreement to label products would be unlikely to be agreed among all manufacturers. This raises the issue as to whether labelling should be a statutory requirement. The mechanism by which an individual can contract L. longbeachae infection from compost and growing media is not currently known but is assumed to be through inhalation of aerosolised dust or contaminated water. Cluster of Legionella longbeachae cases in Scotland in September/October

8 3. Investigation 3.1 Timeline This investigation was carried out from August to October The timeline below summarises the main events during the course of this investigation. Table 1 contains summary case characteristics and should be referred to when reading this section. Week of 19 August 2013 On 22 August Case 1 was confirmed by culture with L. longbeachae infection. Case 1 was male and in the ageband years, who had been admitted to ICU in NHS Lothian on 18 August with community acquired pneumonia and a history of shortness of breath, haemoptysis and cough. This case required ventilation. This case has previously been treated in primary care, prescribed antibiotics and sent home. Investigation identified that this case was a keen gardener. Week of 26 August 2013 On 30 August Case 2 was diagnosed by culture with L. longbeachae infection. Case 2 was a year old female who was admitted to ICU in NHS Lothian 22 August. This case had community acquired pneumonia with a history of diarrhoea and vomiting from one week before being admitted. This case required ventilation. Investigation identified that this case was a keen gardener. Week of 2 September 2013 On 5 September Case 3 was diagnosed by PCR as Legionella species positive. This case was a year old male who had been admitted to hospital in NHS Lothian on 2 September with community acquired pneumonia. This case had previously been admitted to hospital on 29 August 2013 with community acquire pneumonia and discharged on 31 August following antibiotic treatment. On 2 September this case was admitted to ICU and required ventilation. This case was identified as a keen gardener. Following this cluster of cases of the same organism in such a short period of time, NHS Lothian swiftly alerted HPS and local clinicians. On 6 September a letter was circulated to local clinicians and microbiological services increasing their index of suspicion. Case 3 was confirmed by culture on 6 September. Week of 9 September 2013 On 10 September Case 4 was diagnosed by PCR as Legionella species positive in NHS Lothian. This case was a year old female who had been admitted to hospital in NHS Lothian on 7 September with community acquired pneumonia. This case was admitted to ICU and required ventilation. This case was identified as a keen gardener. In NHS Tayside, Case 5 was confirmed by culture with L. longbeachae infection on 9 September. Case 5 was a year old female, who was admitted to ICU with community acquired pneumonia on 3 September. This case was identified as a keen gardener. NHS Tayside informed HPS of this case on 11 September. 4 Cluster of Legionella longbeachae cases in Scotland in September/October 2013

9 On 12 September NHS Lothian held a PAG and requested that HPS attend, who in turn invited NHS Tayside to participate. At this PAG it was agreed that an Incident Management Team (IMT) should be formed to investigate and manage this cluster of cases and given that more than one NHS board was involved, the role of co-ordinator was passed to HPS. HPS actions taken from this meeting involved sharing a modified enhanced surveillance form, starting a line listing and developing an outbreak database, developing case definitions, producing an alert for all NHS boards and developing reactive media lines. Week of 16 September 2013 On 16 September Case 6 was diagnosed as Legionella species positive by PCR at SHLMPRL, on a sample sent by NHS Tayside. On 17 September Case 6 was confirmed as L. longbeachae infection, by culture. Case 6 had been admitted to hospital in NHS Tayside with community acquired pneumonia on 13 September. This case was a year old male, who also required ventilation in ICU. This case was not a keen gardener, but had recently spent time helping his wife digging and planting in their garden. On 18 September, HPS chaired the first IMT, with NHS Lothian, NHS Tayside, relevant local authorities, local and reference microbiology services, Scottish Government and PHE in attendance. The main actions from this meeting were based around the environmental investigation being undertaken and tracing of growing media used by the cases during their two week potential incubation period. Week of 23 September 2013 Environmental Health Officers (EHOs) from the relevant local authorities met on 24 September to discuss best practice in respect to tracing growing media products, sampling methods and disposal of samples. Consensus was met and the need to develop a fuller sampling protocol following this investigation was agreed. A second IMT was held on 26 September. Week of 30 September 2013 A further IMT was held on October 2nd, where full clinical and environmental microbiological investigation results were discussed. No further cases had been identified for around two incubation periods following the date of onset of Case 6. It was agreed that no further investigation was required, but a further meeting including a de-brief session should be held when remaining details had been finalised. Week of 7 October 2013 Case 7 was identified in NHS Lothian. This case was male aged years and was treated for pneumonia by his GP, in the community. This case was a keen gardener. The GP requested blood for immunological investigation after reading about the cluster of cases the first serum sample had elevated titre, so this case was diagnosed following successful antibiotic treatment. A number of repeat blood samples were taken to identify a four-fold change in titre (decrease from 1:128 to 0) for this case. Cluster of Legionella longbeachae cases in Scotland in September/October

10 Week of 25 November 2013 A final IMT was held on 27 November, when the investigation was summarised and final results collated. The IMT was officially closed. It was agreed that Case 7 should be included in the cluster as a probable case. A de-brief session was held. 3.2 Epidemiological investigation The epidemiological investigation for each case was undertaken by Health Protection Nurses within NHS Lothian and Tayside Health Protection Teams and by EHOs in the relevant local authorities. Following the submission of the standard legionellosis surveillance form, a trawling questionnaire developed by HPS following the IMT investigation into cases of L. longbeachae investigation in , was administered to the case or if they were still severely unwell a close relative, followed up by a further interview when the case was fit enough to respond personally. This trawling questionnaire was used for the first time in this investigation. Additional questions were added to this form following its use for the first two cases. This form contained questions about water, soil and growing media exposures, types of gardening activity and hand hygiene practice in the garden and following gardening. Completed forms were sent to HPS who collated them, entered them into an outbreak database and reviewed descriptive epidemiology, which was subsequently reviewed by the IMT. The main case characteristics are detailed in Table Case definitions The case definitions (corresponding to ECDC case definitions) used by the IMT were: Confirmed case clinical or radiological evidence of community acquired pneumonia with disease onset on or after 1 August 2013 AND evidence of having been exposed in Scotland to horticultural growing media (including composted material produced locally or domestically) in the 14 days prior to the onset of symptoms AND isolation of Legionella longbeachae from respiratory secretions Probable case clinical or radiological evidence of community acquired pneumonia with disease onset on or after 1 August 2013 AND evidence of having been exposed in Scotland to horticultural growing media (including composted material produced locally or domestically) in the 14 days prior to the onset of symptoms AND detection of Legionella species specific nucleic acid in respiratory secretions (accompanied by a negative urinary antigen test), or a detected change in Legionella longbeachae serum antibody levels of at least fourfold, or a single high titre of Legionella longbeachae serum antibody Possible case clinical or radiological evidence of community acquired pneumonia with disease onset on or after 1 August 2013 AND 6 Cluster of Legionella longbeachae cases in Scotland in September/October 2013

11 evidence of having been exposed in Scotland to horticultural growing media (including composted material produced locally or domestically) in the 14 days prior to the onset of symptoms AND no current microbiological evidence as to the causal agent Descriptive epidemiology This cluster of cases, for the purposes of investigation, was treated as a single All-Scotland cluster as all cases were linked to the same time period. However, it is acknowledged that in space, there were two separate clusters, one within Lothian and the second within Tayside. Distribution by case definition This cluster consisted of seven cases, including six confirmed cases and one probable case. Distribution by severity of illness All confirmed cases were severely unwell and required hospitalisation and ventilation in ICU. The probable case had milder illness and was treated in the community by primary care. All cases survived. Further details are available in Table 2. Distribution by age/sex The cases included three females and four males. The mean age was 67.7 years (range years). The median age was 71 years. Distribution by place Cases were in two NHS board regions NHS Lothian and Tayside. Cases were distributed across four local authority areas Angus, East Lothian, Edinburgh City and West Lothian. Five of the cases were retired and were not exposed to high or medium risk sources outside their own home and garden. 5 The cases were not known to each other and had not visited the same places. Table 1: Summary of case characteristics Number of cases 7 Case type 6 confirmed and 1 probable Date of onset 11/08/2013 to 11/09/2013 Sex Age Organism Smoker? 4 male and 3 female years Legionella longbeachae 1 2 smokers 3 exsmokers 2 nonsmokers Relevant hobbies Gardening Table 2: Summary of dates of onset, admission and reporting of cases Number of cases Case type Date of onset Date of admission Ward type Length of stay in hospital Date reported Days from onset to diagnosis 7 6 confirmed and 1 probable 11/08/2013 to 11/09/ /08/2013 to 13/09/ ICU (1 not hospitalised) days 23/08/2013 to 10/10/ days for those hospitalised 30 days for case not hospitalised Cluster of Legionella longbeachae cases in Scotland in September/October

12 Distribution by date of onset The epidemiological curve by date of onset is presented below in Figure 1. Cases were clustered over a calendar month, between 11 August and 11 September Figure 1: Epidemiological curve for this cluster of L. longbeachae cases (by date of onset) /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /08/ /09/ /09/ /09/ /09/ /09/ /09/ /09/ /09/ /09/ /09/ /09/2013 Distribution by risk factors 5/7 cases had significant morbidity and underlying risk factors which may contribute to underlying immunosuppression (for one case risk factors were not known). One case was a smoker, three were ex-smokers and one was an occasional smoker. Two cases were not smokers. Distribution by potential exposure Potential exposures were categorised as: travel and stay away from home; hospitalisation; Jacuzzi/whirlpool spas; Showers; Use of water sprays in the garden; Use of soils/growing media/composts/manures/bark/mulches; Handling of recently purchased plants. Lifestyle and occupation None of the cases had a stay away from home, through travelling or in hospital, in the two weeks prior to onset. None of the cases had used a shower other than that in their own home; and none of the cases had used a Jacuzzi or whirlpool spa in the two weeks prior to onset. None of the cases reported recent works on the water systems within their homes. All cases were interviewed about potential exposures to water, growing media, soil and other garden products in their home and garden. All seven cases had spent time in the garden or outdoors in the two weeks prior to onset. 4/7 cases had exposure to water spray in the garden this included use of garden taps, hoses and electric garden fountains. One case had an irrigation 8 Cluster of Legionella longbeachae cases in Scotland in September/October 2013

13 or sprinkler system, which was located in a potting shed. No cases collected rainwater in butts for use on the garden. There is evidence to suggest that dripping hanging baskets can increase risk of legionellosis. 14 4/7 cases had hanging baskets which hung outside. For 2/4 cases, these hanging baskets dripped when they were watered. Use of growing media and related gardening practices Possible infection pathways from a contaminated source (growing media) to case were hypothesised. The route of infection might include a case breathing in growing media dust or contaminated water vapour whilst handling contaminated growing media. It is likely that handling growing media indoors or in an enclosed space can lead to a build up of contaminated aerosol/ particles around the user. Alternatively it is possible that contaminated growing media could be passed from hand to face/mouth/nose where it is inhaled (or ingested). 6/7 cases had recently bought growing media and had used it in the two weeks prior to onset. No cases had used farm produced compost or manure. One case had a garden compost heap, but had not disturbed the heap during the two weeks prior to onset. 6/7 cases used growing media/potted outside; one case used growing media/potted in the greenhouse/potting shed; and 2/7 cases used growing media/potted in the house. 4/7 cases wore gloves whilst using growing media. No cases wore a mask whilst using growing media. 5/7 cases had access to hand washing facilities close to where they worked with growing media; and washed their hands before undertaking other activities. 2/7 cases ate, drank or smoked whilst undertaking gardening activities. Analytical study No analytical study was undertaken in relation to this cluster. This was discussed at IMT meetings, but the number of cases was deemed too small. 3.3 Clinical microbiological investigation All local diagnostic laboratories in Scotland provide urinary antigen testing for Legionella, which will detect L. pneumophila Sg1; and all provide a culture service and refer Legionella isolates to SHLMPRL for further characterisation. One diagnostic laboratory (NHS Lothian Department of Laboratory Medicine, based at the Royal Infirmary of Edinburgh) also uses two molecular screening tests for Legionella specifically PCR for L. pneumophila and a second for Legionella species (that is all species except L. pneumophila). These tests were introduced in SHLMPRL provides a reference service for samples from across Scotland. For cases of Legionnaires disease to be confirmed in Scotland all positives are verified by SHLMPRL. Specific tests offered by SHLMPRL include: a variety of urinary antigen tests; PCR tests specific for L. pneumophila Sg1, other L. pneumophila serogroups and Legionella species (all species except L. pneumophila); serology testing with a wide range of species specific antibodies; and strain typing. It is well recognised that L. longbeachae cases test negative with urinary antigen testing, which may be used by some clinicians as a test to rule out legionellosis. Diagnosis of L. longbeachae infection requires respiratory samples (for example sputum or broncho-alveolar lavage) to test positive for Legionella species by PCR or culture; or for blood samples to have an elevated titre Cluster of Legionella longbeachae cases in Scotland in September/October

14 to L. longbeachae specific antibody. Following urinary antigen testing which is negative, additional samples may not be requested. Clinical microbiology testing results are summarised in Table 3. Detection in NHS Lothian Cases 1-4 were detected in NHS Lothian principally though the PCR screening test employed in the diagnostic laboratory. Samples taken early in the hospital stay for each case met the laboratory criteria for testing of lower respiratory samples by PCR (community acquired pneumonia, severe illness, unknown exposure) and tested positive for Legionella species. In all cases, samples were forwarded to SHLMPRL for confirmation and any remaining sample was cultured. Colonies obtained by culture were characterised by SHLMPRL. The positive PCR test informed the clinical management of the cases before confirmation of strain species was available. These cases may not have been identified if this PCR test was not used in the local diagnostic laboratory. Case 7 was detected after recovery from illness using serological confirmation. It is likely that this case would not have been detected if information materials had not been circulated to NHS Lothian primary care clinicians. Detection in NHS Tayside Cases 5 and 6 were detected in NHS Tayside though culture and additionally for Case 6, by PCR for Legionella species at SHLMPRL. At the time of this cluster, NHS Tayside did not use Legionella PCR tests. Instead in cases of severe community acquired pneumonia, where possible, samples are taken for a broad range of bacterial culture. In these cases, positive cultures were sent to SHLMPRL for characterisation. Culture positivity informed clinicians of treatment options. Characterisation at SHLMPRL All positive PCRs, cultures and sera pertaining to these cases were forwarded to SHLMPRL for further characterisation. Results are summarised in Table 3. Table 3: Summary of clinical microbiology testing results for cases Case Urinary antigen test L. pneumophila PCR Legionella species PCR Culture Serology (L. longbeachae specific antibody response) 1 negative negative positive positive four-fold rise 2 negative negative positive positive four-fold rise 3 negative negative positive positive four-fold rise 4 negative negative positive positive single high titre 5 negative negative * positive * 6 negative negative positive positive single moderate titre 7 negative * * * four-fold fall Organism L. longbeachae serogroup 1 L. longbeachae serogroup 1 L. longbeachae serogroup 1 L. longbeachae serogroup 1 L. longbeachae serogroup 1 L. longbeachae serogroup 1 L. longbeachae serogroup 1 (* = test not undertaken) 10 Cluster of Legionella longbeachae cases in Scotland in September/October 2013

15 All cases were identified as having L. longbeachae Sg1 infections. All tested negative by urinary antigen testing and by L. pneumophila specific PCR (where tests were undertaken). Where tested, all Legionella species PCR was positive. Where tested all showed elevated titres to L. longbeachae specific antibody. 3.4 Environmental investigation Environmental investigation was undertaken by EHOs within the relevant local authorities. In some instances, EHOs interviewed cases and completed the trawling questionnaire. EHOs undertook a risk assessment of cases homes and garden with respect to water and soil / growing media / compost exposures. Where a risk was identified, if possible a sample was taken for microbiological analysis. Results of the investigation and sampling are summarised in Table 4. Field investigation of cases homes and gardens Visits were made to the homes of cases, and for one case in addition their own holiday home where they had stayed during their incubation period. The water systems within homes were investigated and deemed low risk for all cases. No domestic hot and/or cold water samples were taken. All cases had relevant exposures within their gardens. However, for one case this was deemed low risk as no water, soil, growing media or compost had been handled. Water sources within gardens were investigated and deemed low risk for a further two cases. For four cases, aerosol producing water sources had been used within the garden (garden hoses and garden fountain). However, as the water source was mains cold water, this was deemed low risk and no water samples were taken. For 6/7 cases, bagged shop-bought growing media had been handled directly in the two week incubation period, in some cases together with garden soil or bark mulch. Where bagged growing media remained, the bag was removed and samples provided for microbiological testing. In one case, all growing media that had been handled had been dug into the garden as soil improver around newly planted shrubs. In this instance samples of soil/growing media mix were taken from the ground at the site of planting. All cases who had used bags of growing media in the two weeks prior to onset, had stored the bags in the period between purchase and use. 5/6 cases had stored the bags of growing media inside (the house) or undercover (garage, garden shed, greenhouse or polytunnel). Tracing of products from retail outlets Cases provided details of purchase of the bagged growing media, including rough dates and place of purchase. All products were bought at different times in the period end of July to mid- September and from different premises. EHOs used the packaging and barcode to identify manufacturer and sites of manufacture. Five different manufacturers were identified, in five different sites based in England, Scotland, Northern Ireland and Ireland. Manufacturers were contacted to identify dates of production and composition of the growing media. The IMT agreed that as no single site was implicated, further investigation into sources of composted material (which was the most likely source of L. longbeachae contamination) 12 was unnecessary, as it is understood that composting sites supply to local growing media manufacturers, due to high transport costs for this product. 12 Cluster of Legionella longbeachae cases in Scotland in September/October

16 Table 4: Summary of results of environmental investigation Case Water samples from house Water samples from garden Soil/ growing media/ compost samples taken Growing media brand(s) Retail outlet Manufactured where? Composition Growing media test results Storage of growing media at home prior to use 1 No No Yes 1. Topsoil 2. General purpose compost Large chain Northern garden centre Ireland 1. Topsoil: Mixture of soil and a small percentage (not specified) of composted tree bark from local Northern Ireland supplier. 2. Compost: Mixture of peat, woodfibre (produced by manufacturer), lime and fertiliser. 1. Topsoil: L. longbeachae serogroup 1 isolated. 2. Compost: negative. yes, stored in house 2 No No Yes Multi-purpose Compost Independent England garden centre Mixture of composted bark fines (45%), retail grade peat (20%), green compost (35%), Dolodust (0.05 %), base nutrients (0.24%), wetting agent (0.06%). Manufactured on 6 November Suppliers of green compost are all local and in England or Scotland. L. longbeachae serogroup 1 isolated yes, stored in garden shed 3 No No Yes Multi-purpose Compost Independent Scotland garden centre Composition unknown. Manufactured on 28 May Single local source of green compost. L. longbeachae serogroup 1 isolated yes, stored in garage 4 No No No No No Yes 6 No No Yes 7 No No Yes 1. Fruit and vegetable compost 2. Bark mulch Multipurpose compost - all media in bag dug into soil at site of new planting, samples taken from this site (soil/compost mixture) Enriched compost Large chain 1. Scotland garden centre 2. Bark mulch: manufacturer unknown Large chain Ireland garden centre Independent England garden centre 1. Fruit and veg compost: mixture of peat, wood fibre, green compost, Dolomitic lime, inorganic nitrogen and phosphorus. Mixture of moss peat, green compost & coir, Dolomitic lime, wetting agent. Green compost produced by manufacturer. Mixture of green compost, woodfibre, composted bark fines, coir, fertilisers and limestone. Manufactured on October Green compost supplied by local producer. 1. Compost: L. longbeachae serogroup 1 isolated 2. Bark mulch: tested negative L. longbeachae serogroup 1 isolated Tested negative yes, stored in greenhouse yes, stored in polytunnel yes, stored in garden shed 12 Cluster of Legionella longbeachae cases in Scotland in September/October 2013

17 3.5 Environmental microbiology investigation Samples of growing media and other garden samples taken from the homes of the cases were sent to Edinburgh Scientific Services (ESS) or Tayside Scientific Services (TSS) for microbiological testing. The main test employed by the laboratories is microbiological culture a test which can take up to ten days to complete (given the number of bacteria present in a sample can be very small). In addition, ESS also employs PCR tests for detection of the presence of Legionella; specifically these are separate tests for L. pneumophila and Legionella species. Where PCR results were positive or where colonies were obtained, these were forwarded to SHLMPRL for further characterisation. SHLMPRL employs a number of sensitive molecular techniques (including PCR techniques) which the scientific services do not and in some cases worked directly on the environmental samples in order to better characterise them. The samples taken and summary of results is given in Table 4. For testing of growing media and other garden samples, five out of eleven samples tested were positive for L. longbeachae Sg1. This equates to five samples linked to five confirmed cases. In each matched pair of clinical and environmental samples, the same strain of Legionella (L. longbeachae Sg1) was identified. 3.6 AFLP typing All isolates were investigated using AFLP (amplified-fragment length polymorphism) typing at SHLMPRL. This technique uses PCR to amplify specific sections of the organism genome, which are then sequenced fully and the sequencing compared for homology. This technique is usually applied to L. pneumophila genome and there is very little information available for L. longbeachae genome comparison. This means that interpretation of these results for L. longbeachae is difficult. This typing indicated that there were three types of L. longbeachae Sg1 (AFLP types 1, 2 and 3), as had been seen before in Scotland in samples from previous cases. Where clinical and linked environmental samples were available, in all cases the same AFLP type was identified for the case and the compost they had been exposed to during their incubation period. 3.7 Whole genome sequencing The L. longbeachae isolates from the patients in this cluster and from the growing media linked to them were subjected to whole genome sequencing (WGS). This work was carried out at Edinburgh University by Professor Ross Fitzgerald in collaboration with SHLMPRL. Three or four separate isolates from individual patients were included where they were available; it was desirable to do this also for multiple isolates from the same bag of growing medium but they were not often available. A number of other Scottish isolates of L. longbeachae obtained by the SHLMPRL in the last ten years were also included. In the analysis of a cluster of cases WGS can be regarded primarily as a fine typing method, with great discriminatory power but it also has considerable ability to help elucidate the population structure of L. longbeachae. Considerable diversity is seen among the isolates with a complex population structure showing many subgroups. Wherever multiple isolates from the same patient were sequenced they were shown to be almost completely identical. This is an important control observation as it validates the dataset and confirms that a single strain is responsible for causing disease in each patient. Cluster of Legionella longbeachae cases in Scotland in September/October

18 The isolates from this cluster are no more closely related to each other than to other Scottish isolates in the last ten years and the information available suggests that the Scottish isolates are themselves a diverse collection. Additionally we have not found any close relationship between patients isolates and those from the samples of growing media that they had been working with. Whatever the cause of the cluster it does not appear to be due to the emergence of a new strain in commercially produced growing media. 14 Cluster of Legionella longbeachae cases in Scotland in September/October 2013

19 4. Risk management 4.1 Prevention of further exposure to hazardous agent Based on the epidemiological investigation (which identified 6/7 cases with exposure to recently purchased growing media) and the microbiological investigation (which identified the same species of Legionella in the patient and the growing media they were exposed to in 5/6 of these cases), the IMT agreed that this exposure was high risk for this infection for these cases. However, the environmental investigation did not identify a common retail outlet, a common manufacturer, a common manufacturing site or a common source or components used in the manufacturing process. Aside for providing general hygiene advice for user of growing media, the IMT took no further action in terms of preventing further exposure to sources of the hazardous agent as it appeared to be present in multiple sources. Although this cluster was unprecedented in Scotland in terms of the number of concurrent cases, the overall risk of illness remains low. The incidence in 2013 was 1.64 cases of L. longbeachae infection per million population in Scotland (up from the annual incidence of less than 1 case per million population in Scotland for the years ). Given the volume of growing media products and compost sold and the large number of gardeners in Scotland, the risk of being infected with this organism following exposure to contaminated growing media appears to be very low Care of cases The six confirmed cases were all severely unwell and required intensive care and ventilation. Periods of stay in hospital are detailed in Table 2. Cluster of Legionella longbeachae cases in Scotland in September/October

20 5. Risk communication 5.1 Communication with clinicians Following the identification of the first three cases, NHS Lothian circulated a letter to local clinicians, which detailed that three cases of unusual Legionnaires disease had been identified concurrently, caused by L. longbeachae. Symptoms were detailed and links with gardening and exposure to growing media were indicated. Following the PAG on 12 September, HPS sent out a briefing note to all NHS board HPTs detailing the NHS boards affected, symptoms, microbiology testing results and types of test and samples to submit. This briefing note also provided general advice about garden hygiene and case definitions for the suspected outbreak. It was requested that HPTs consider cascading the briefing note to all clinicians and to local authority Environmental Health Teams. This briefing note was also forwarded to PHE, PHW, PHNI and CMO Office in Scottish Government. ECDC was also informed by to the ELDSNet Team. No European Alert was issued due to the local nature of the cluster and suspected source(s). In addition, on 12 September, NHS Tayside sent a letter to local clinicians with details of the cluster, symptoms, illness identified as slow onset of respiratory illness and links with gardening and exposure to growing media were indicated. A further briefing note was sent to all NHS boards HPTs following the first IMT meeting chaired by HPS on 18 September. In this note, a situation update was provided; updated general advice about garden hygiene; and actions for cascade to local authorities and microbiology departments; and points of contact within HPS for epidemiological and environmental investigation coordination. No further communications were sent to clinicians. 5.2 Communication with the public HPS did not receive any direct enquiries from members of the public. Following the PAG on 12 September, HPS, NHS Lothian and NHS Tayside prepared a press release which highlighted the cluster of cases in NHS Lothian. This was released by NHS Lothian. This press release also indicated that this type of infection was known but rare, and highlighted the importance of general good hygiene practice whilst gardening. No further specific risks could be highlighted as there was no common retail outlet, product or manufacturer. At the IMT on 18 September, it was agreed that HPS would be the principal contact for information about the cluster and would handle national press enquiries. Any specific queries about cases were referred to the appropriate press departments in NHS Lothian or NHS Tayside. Following the proactive press release on 13 September there was significant media interest in this cluster of cases. The IMT Chair, Dr Martin Donaghy, gave interviews with BBC and ITV news. Reporters from national and local papers rang HPS for further information. Following every IMT, the press statement was revised and updated. However, following the initial proactive release by NHS Lothian on 13 September, all following revisions of the statement were reactive only. Following revision of the press statement after the IMT, it was circulated to all IMT members to ensure consistency of message across NHS Boards and local authorities. 16 Cluster of Legionella longbeachae cases in Scotland in September/October 2013

21 5.3 Communication with retailers Following the press release on 13 September, HPS was approached by a major garden centre chain, who wanted to provide their customers with reassurance for purchases of growing media. HPS prepared a short paragraph highlighting good garden hygiene with respect to growing media handling, see Figure 2 below. This statement was provided without HPS or NSS branding, so that retailers could amend wording and add their own branding. The garden centre chain was content with this statement and displayed it at cash till points throughout their garden centres. It was agreed by the IMT that this statement for proactive use only and would be shared with other retailers only if they approached HPS for advice. No other retailer did this. 5.4 Communication with manufacturers Following development of text highlighting general garden hygiene for use by retailers (see Figure 2) this was shared with representatives of the Growing Media Association (GMA). The GMA had been in touch with NHS Lothian HPT and local authority EHOs during the course of the environmental investigation, to offer full support and collaboration in terms of tracing products and manufacturing sites with their member manufacturers. The text developed for retailers was shared with the GMA after it had been released to the major garden centre chain. Figure 2: Text developed for retailers to display at point of sale of growing media Gardening Good Hygiene A few simple good hygiene tips can help you during gardening: Wear gloves. Wear a dust mask if you are working on anything dusty, particularly indoors. Wash your hands as soon as you finish. If you are going to smoke, wash your hands before doing so. Storing and Handling Compost, Potting Mix, Mulches and Soil As well as the general advice above, the following advice can help you avoid breathing in dust: Store compost, potting mixes, mulches and soil in a cool place, away from the sun. Open any bags carefully in a well ventilated area and if possible using a safety blade or sharp knife. Keep the door or a window open in greenhouses or sheds when potting-up plants or filling hanging baskets. Wear a dust mask if you are working on anything dusty, particularly indoors. Cluster of Legionella longbeachae cases in Scotland in September/October

22 The GMA strongly disagreed with the lines in the HPS advice detailing use of a mask in certain circumstances. The GMA felt this was strongly disproportionate to the risk, and possibly even alarmist. The GMA followed this with release of a statement to the members of the Horticultural Trades Association (HTA), highlighting general garden hygiene and not including details about wearing a mask. The GMA statement is detailed in Figure 3. Figure 3: Statement released by the GMA to members of the HTA Legionella longbeachae in Growing Media There have been reports of five more cases of Legionella with links to growing media in Scotland. The Growing Media Association takes this issue very seriously and has offered its full cooperation with NHS Lothian in its investigation into the source of the contamination. In the meantime, the HTA and the GMA would like to reassure garden centres and their customers that the risk of infection is extremely low. This was confirmed by a recent report by Health Protection Scotland which recorded less than one case per million population per year between Of the small number of infections diagnosed, those most at risk are those undertaking gardening activities indoors, and is greatest in those aged over 55 who smoke or have underlying chronic, medical conditions. Compared with the number of gardeners in Scotland and the volume of growing media used, the HPS report concludes that the risks of severe disease are very low. However, to reduce these risks further, we recommend that gardeners follow sensible hygiene precautions. These include: Wearing gloves Washing hands after all gardening activity, particularly before eating, drinking or smoking. 20 September Cluster of Legionella longbeachae cases in Scotland in September/October 2013

23 6. Discussion and conclusion 6.1 Discussion The cluster of Legionnaires disease cases described in this report is the first such cluster identified in Scotland caused by L. longbeachae Sg1 infection. Other cases of Legionnaires disease caused by L. longbeachae had been identified in Scotland before this cluster (eleven cases in the period ), but cases had always been sporadic in nature. 12 Clustering of seven cases with dates of onset over a period of one calendar month, in a small geographical area, prompted the investigation detailed here. Although no common source of infection was identified for these cases, this investigation was warranted due to the severity of the illness and the potentially large number of Scottish residents exposed to the contaminated source. The sections below identify and discuss key findings of this investigation. Case ascertainment Cases in this cluster were identified in two different NHS board regions, each with their own diagnostic microbiology service. The cases were detected using different microbiology techniques, which correspond to different clinical and microbiological protocols in place in each NHS board. For NHS Lothian, clinical protocols for management of those admitted to respiratory, high dependency or ICU with community acquired pneumonia, alerts clinicians to take a lower respiratory tract sample (sputum or broncho-alveolar lavage) for a range of PCR tests including those for L. pneumophila and Legionella species. Cases 1-4 in NHS Lothian were detected as they were positive (unusually) for Legionella species. The sputum samples were then cultured and referred isolates were identified by SHLMPRL as L. longbeachae Sg1. A positive PCR result for Legionella species prompted alternative clinical treatment options more quickly than the culture and identification of the organisms, as this is more prolonged for Legionella species. For NHS Tayside, clinical protocols for management of those admitted to high dependency or intensive care units with community acquired pneumonia, alert clinicians to take a saliva/sputum or broncho-alveolar lavage sample for a wide range of bacterial culture including on media specific for Legionella bacteria. This is not routine in all NHS boards to our knowledge. This local diagnostic service did not offer PCR for Legionella at the time of these cases. Subsequent colonies were identified by SHLMPRL as L. longbeachae Sg1, Case 5 was identified in this way and Case 6 was confirmed in this way. Although culture takes longer than PCR, the presence of Legionella colonies does prompt clinical treatment options, even though it took additional time to identify the responsible strain of Legionella. Case 7 was identified by serology following treatment and recovery. It is unlikely that this case would have been identified if NHS Lothian had not circulated information about the cluster to clinicians (including primary care) and there had not been articles in the media. Serological detection of immune response to Legionella infection is only carried out at SHLMPRL and this service is available for samples from patients Scotland-wide. However, awareness that this service is available is perhaps less widely known and is certainly an unusual request from primary care clinicians. The use of serology was highlighted in the letter circulated to clinicians in NHS Lothian and NHS Tayside and this probably lead to the detection of this case. Cluster of Legionella longbeachae cases in Scotland in September/October