3. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 i
Table of Contents
Abbreviations-ii
1. Introduction 1
2. Background 2
2.1 Legionella bacteria and legionellosis 2
2.2 Legionnaires’ disease in Scotland 2
2.3 Legionnaires’ disease caused by L. longbeachae 2
3. Investigation 4
3.1 Timeline 4
3.2 Epidemiological investigation 6
3.3 Clinical microbiological investigation 9
3.4 Environmental investigation 11
3.5 Environmental microbiology investigation 13
3.6 AFLP typing 13
3.7 Whole genome sequencing 13
4. Risk management 15
4.1 Prevention of further exposure to hazardous agent 15
4.2 Care of cases 15
5. Risk communication 16
5.1 Communication with clinicians 16
5.2 Communication with the public 16
5.3 Communication with retailers 17
5.4 Communication with manufacturers 17
6. Discussion and conclusion 19
6.1 Discussion 19
6.2 Conclusion 22
7.Lessons learned and recommendations 24
7.1 Lessons learned 24
7.2 Recommendations 24
8. References 26
9. Appendices 27
9.1 Members of the national IMT 27
4. ii Cluster of Legionella longbeachae cases in Scotland in September/October 2013
Abbreviations
ECDC European Centre for Disease Prevention and Control
ELDSNet European Legionnaires’ Disease Surveillance Network
ESS City of Edinburgh Council Scientific Services
GMA Growing Media Association
HPN Health Protection Network
HPS Health Protection Scotland
HPT Health Protection Team
HTA Horticultural Trades Association
IMT Incident Management Team
ICU Intensive Care Unit
NHS National Health Service
NHS NSS NHS National Services Scotland
PAG Problem Assessment Group
PCR Polymerase Chain Reaction
PHE Public Health England
PHNI Public Health Northern Ireland
PHW Public Health Wales
Sg1 Serogroup 1
SHLMPRL Scottish Haemophilus, Legionella, Meningococcus, Pneumococcus Reference
Laboratory
TSS Dundee City Council Tayside Scientific Services
WGS Whole Genome Sequencing
5. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 1
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 2008-2013. 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.
6. 2 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
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 community-
acquired 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 20082
. 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 (ECDC3
) through the European Legionnaires’ Disease Surveillance
Network (ELDSNet4
). 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 Sg1.
2.3 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
7. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 3
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 bacteria10
– 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
legislation13
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
100.15
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. longbeachae16
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.
8. 4 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
3. Investigation
3.1 Timeline
This investigation was carried out from August to October 2013. 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 80-90 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 70-80
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
60-70 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 70-80 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 50-60 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.
9. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 5
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 70-80 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 50-60 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.
10. 6 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
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 201212
, 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 1.
3.2.1 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
11. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 7
• 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
3.2.2 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 50-90
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
Case type
Date of
onset
Sex Age Organism Smoker?
Relevant
hobbies
7
6 confirmed
and 1
probable
11/08/2013
to
11/09/2013
4 male and
3 female
50-90 years
Legionella
longbeachae
1
2 smokers
3 ex-
smokers
2 non-
smokers
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
11/09/2013
18/08/2013
to
13/09/2013
6 ICU (1 not
hospitalised)
11-43 days
23/08/2013
to
10/10/2013
7-16 days for those
hospitalised
30 days for case not
hospitalised
12. 8 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
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 2013.
Figure 1: Epidemiological curve for this cluster of L. longbeachae cases (by date of onset)
0
1
10/08/2013
11/08/2013
12/08/2013
13/08/2013
14/08/2013
15/08/2013
16/08/2013
17/08/2013
18/08/2013
19/08/2013
20/08/2013
21/08/2013
22/08/2013
23/08/2013
24/08/2013
25/08/2013
26/08/2013
27/08/2013
28/08/2013
29/08/2013
30/08/2013
31/08/2013
01/09/2013
02/09/2013
03/09/2013
04/09/2013
05/09/2013
06/09/2013
07/09/2013
08/09/2013
09/09/2013
10/09/2013
11/09/2013
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
13. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 9
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 2010.
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
14. 10 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
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)
Organism
1 negative negative positive positive four-fold rise
L. longbeachae
serogroup 1
2 negative negative positive positive four-fold rise
L. longbeachae
serogroup 1
3 negative negative positive positive four-fold rise
L. longbeachae
serogroup 1
4 negative negative positive positive single high titre
L. longbeachae
serogroup 1
5 negative negative * positive *
L. longbeachae
serogroup 1
6 negative negative positive positive single moderate titre
L. longbeachae
serogroup 1
7 negative * * * four-fold fall
L. longbeachae
serogroup 1
(* = test not undertaken)
15. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 11
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
16. 12 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
Table 4: Summary of results of environmental investigationCase
Watersamplesfromhouse
Watersamplesfromgarden
Soil/growingmedia/compost
samplestaken
Growingmediabrand(s)
Retailoutlet
Manufacturedwhere?
Composition
Growingmediatestresults
Storageofgrowingmediaat
homepriortouse
1 No No Yes
1. Topsoil
2. General
purpose
compost
Large chain
garden centre
Northern
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
garden centre
England 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
2012. 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
garden centre
Scotland Composition unknown.
Manufactured on 28 May
2013. Single local source of
green compost.
L. longbeachae
serogroup 1
isolated
yes, stored in
garage
4 No No No - - - - - -
5 No No Yes
1. Fruit and
vegetable
compost
2. Bark mulch
Large chain
garden centre
1. Scotland
2. Bark
mulch:
manufacturer
unknown
1. Fruit and veg compost:
mixture of peat, wood fibre,
green compost, Dolomitic
lime, inorganic nitrogen and
phosphorus.
1. Compost:
L. longbeachae
serogroup 1
isolated
2. Bark mulch:
tested negative
yes, stored in
greenhouse
6 No No Yes
Multipurpose
compost - all
media in bag dug
into soil at site
of new planting,
samples taken
from this site
(soil/compost
mixture)
Large chain
garden centre
Ireland Mixture of moss peat, green
compost coir, Dolomitic
lime, wetting agent.
Green compost produced by
manufacturer.
L. longbeachae
serogroup 1
isolated
yes, stored in
polytunnel
7 No No Yes
Enriched
compost
Independent
garden centre
England Mixture of green compost,
woodfibre, composted bark
fines, coir, fertilisers and
limestone.
Manufactured on October
2012. Green compost
supplied by local producer.
Tested
negative
yes, stored in
garden shed
17. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 13
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.
18. 14 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
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.
19. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 15
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 2008-2012). 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.12
4.2 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.
20. 16 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
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 email 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 co-
ordination.
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.
21. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 17
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.
22. 18 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
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 2008-2012. 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 2013
23. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 19
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 2008-2013), 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.
24. 20 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
Given that detection techniques for Legionella infections other than L. pneumophila Sg1 (detected
using urinary antigen testing – all diagnostic laboratories hold kits for this) are variable across
diagnostic laboratories, and use of serology is variable across different NHS board regions, it is
likely that ascertainment of cases of community acquired pneumonia caused by Legionella species
is also variable across Scotland. Indeed, it is likely that these cases are under-ascertained. Given
that a confirmed diagnosis of Legionella infection may prompt alternative clinical treatment and is
likely to improve clinical outcome, it is in the best interest of patients to optimise microbiological
confirmation of infection. Accordingly, it is recommended that there is a discussion amongst
diagnostic microbiologists in Scotland as to how best to provide equitable Scotland-wide provision
of appropriate diagnostic tests in the light of emerging pathogenic strains.
Severity of illness
The six confirmed cases in this cluster all had severe illness that required admission to ICU and
ventilation. Severity of illness for Legionnaires’ disease cases is affected by immune status and
other intrinsic risk factors including smoking. 5/6 of the severe cases had underlying medical
conditions which may lead to immunosuppression; the remaining case was a smoker. So, all cases
of severe illness had significant underlying intrinsic risk factors.
Given that gardening is traditionally a hobby for the older generation that is actively encouraged
in “wellbeing” arenas and given the high proportion of the older population who experience
immunosuppression due to underlying illness, it is likely that we will see further cases.
Epidemiological investigation
This cluster was of a small number of cases and as such had limited power to draw epidemiological
conclusions. This cluster used a trawling questionnaire designed by HPS, containing specific
questions about garden exposures and gardening activities. NHS board HPTs and EHOs found this
questionnaire useful, although additional questions were added to it after first use. Results from
the questionnaire were less effective at identifying any specific garden exposures or gardening
activities which were high risk (other than exposure to growing media), due to the small sample
number. To get a better idea of gardening activities which are higher risk, a larger sample is
needed, perhaps in the context of an analytical study.
There is very little information published about the infectious risks of exposure to L. longbeachae.
There is a single case-control study published by New South Wales, Australia14
which highlights
use of potting compost, poor hand hygiene whilst gardening and proximity to dripping hanging
baskets as increasing risk of illness. These findings have influenced the HPS advice regarding L.
longbeachae, but further understanding of particular gardening activities which increase risk, would
be beneficial.
Microbiological investigation
Microbiological investigation identified seven cases of L. longbeachae Sg1 infection, using three
primary techniques – PCR, culture and serology. Where possible, more than one technique was
used to corroborate results. Results from these techniques were consistent across the cases.
Where undertaken: all tested positive for Legionella species by PCR; all were culture positive
for L. longbeachae Sg1; all showed serological response to L. longbeachae Sg1. In addition, all were
negative by urinary antigen testing. Whilst this is to be expected, it reinforces the concern that if
25. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 21
clinical management protocols do not suggest further investigation for Legionella infection following
a negative urinary antigen test result, then cases may not be detected.
Five samples of growing media, linked with five confirmed cases, were L. longbeachae Sg1 positive
by culture. This would suggest that growing media was the likely source of infection in these cases.
The AFLP results suggest that patient and associated environmental strains were indistinguishable.
However whole genome sequencing identified differences between the patient and associated
environmental strains. These results suggest that there is a large amount of heterogeneity in the
strains found in compost and that multiple strains from the same compost would need to be
sequenced to confirm a link. This follows a similar pattern to that encountered in environmental
waters where the most pathogenic strains of Legionella are rarely detected in routine water
sampling until there is a case or an outbreak and even then there are many cases/outbreaks where
the source is never identified.
Environmental investigation
The environmental investigation was undertaken by EHOs in the relevant local authorities (four),
co-ordinated by HPS. Sampling protocols and an understanding of risks were not in place before
this cluster and co-ordination by HPS led to discussion and agreement around best practice. In
order that this is shared more widely, it would be beneficial that this is incorporated into revised
HPN national guidance for Legionella outbreaks and clusters.
In some cases EHOs had difficulty in tracing products as retailers delayed response to or ignored
requests for information. Assistance from the GMA and HTA was welcome in resolving this. This
should be borne in mind for future investigations.
HPS developed generic gardening hygiene advice for the public which was made available to
retailers and was published on the HPS website. This was included in all media releases. This
advice highlighted good garden hygiene in terms of wearing gloves, hand washing and refraining
from smoking whilst handling garden products. In addition, advice included to open bags and use
the contents in a well ventilated area, preferably outdoors and to wear a mask if the material is
dusty.
Co-operation from retailers and manufacturers was generally good. The GMA had reservations
and took a contrary view to HPS in terms of the information provided to retailers for the general
public, specifically about the use of masks. In retrospect, it would have been useful for this to
be discussed and agreed with the GMA before release, as this would have prevented the GMA
releasing its own statement to members which whilst similar, was not the same as the message
from HPS.
Risk management
The investigation undertaken in 2012 into sporadic cases of L. longbeachae highlighted a possible
risk management strategy of placing warning labels on bags of growing media.12
This was discussed
at the Scottish Government at the time but no further action was taken due to existing UK
labelling of bags with generic safety and hygiene advice and insufficient evidence that specific
labelling in Australia and New Zealand had been effective. Another factor taken into account was
the small proportion of cases of Legionnaires’ disease in Scotland caused by L. longbeachae (around
2% of cases) compared with around 50% of cases in Australia and New Zealand.
26. 22 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
This conversation was revisited with Scottish Government and the UK Department of Health
following this cluster. It was agreed that there was still insufficient evidence to take this strategy
forward. However specific steps have been agreed and include that:
1. HPS should develop a hypothesis generating (“trawling”) questionnaire specifically
for L. longbeachae cases and a protocol for the associated environmental investigation
(including sampling). Based on indications from this trawling questionnaire a targeted
investigation may be merited.
2. HPS should explore how best to raise awareness of risk of L. longbeachae infection from
growing media, amongst those with highest risk – older and immunocompromised.
Limitations
Epidemiological investigation was limited due to the small number of cases in this investigation –
this prevented statistical evaluation of risk. Clinical diagnostic practices were different in different
NHS boards and this provided some degree of confounding in terms of case identification.
The relative novelty of Legionnaires’ disease caused by this organism means that standardised
epidemiological and environmental processes were still evolving and were not in place for the
investigation of this cluster.
6.2 Conclusion
This was a cluster of cases in time for which no point source was identified. The reasons for
increased incidence in Lothian and Tayside at this time are unclear.
The growing media linked to five cases in which L. longbeachae Sg1 was identified, came from
different retailers, different manufacturers and was indeed made at sites in different countries.
It is therefore likely that L. longbeachae contamination derives from multiple sources in multiple
countries. This is supported by work which has identified L. longbeachae contamination in a variety
of growing media, composted green waste and soil samples from a wide range of environments.10,11
It is possible that a significant proportion of growing media used in the UK is contaminated with L.
longbeachae; but since very few cases are detected there must be a number of factors influencing
likelihood of infection.
A number of combined factors which may explain this cluster are detailed below.
1. The composting process used to produce composted green waste is conducive for
Legionella growth – elevated temperature and water release. At this time we do not
know if the composting process continues after bagging or after sale.
2. Australia and New Zealand show seasonality in cases of Legionnaires’ disease caused
by L. longbeachae, around times of increased use of growing media. Whilst this is
traditionally in the spring, this cluster occurred at the time when gardeners start to
prepare for the following year with planting of spring plants such as bulbs. Sporadic cases
in Scotland outside this cluster, have not shown seasonality.
3. Immunosuppressed individuals, smokers and those who are older show increased
susceptibility to Legionnaires’ disease. The majority of cases in this cluster meet these
criteria.
27. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 23
4. The majority of cases of Legionnaires’ disease caused by L. longbeachae in Scotland
have been in keen gardeners, who have had significant exposure to growing media.
This includes multiple exposures, prolonged exposure and exposure in enclosed
environments.
5. Climatic conditions may favour Legionella growth after bagging and/or point of sale.
August and September were unusually warm in Scotland in 2013 and storage of bags
post-sale in enclosed spaces (such as inside the home, garage, shed, greenhouse or
polytunnel) may have led to the bags being very warm during the day and protected
from cold nights by being covered. In such conditions, the organism may thrive.
28. 24 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
7. Lessons learned and recommendations
7.1 Lessons learned
A lessons learned exercise was undertaken at the final IMT on November 27th, using a HPS
standard debrief template. The overall view of the IMT was that this investigation had been well
managed and was extensive and thorough. Specific points for further action are highlighted in the
recommendations section.
7.2 Recommendations
A number of recommendations were made in the debrief exercise and a number of outstanding
actions for the IMT were in place following the close of the investigation. These are detailed
below.
Guidance
1. Advice on L. longbeachae infection and investigation into cases should be included in the
HPN Guidance on Legionella cases, clusters and outbreaks in the community (due for
revision in 2014).
2. Sampling protocols should be developed specifically for growing media sampling, which
should also include information about use of masks during sampling. This should be
included in the revised HPN guidance.
Meeting management
3. Make every effort to include all relevant staff as early on in the investigative process as
possible and invite them to all IMT meetings. This will ensure that all agencies are fully
informed at all times.
Investigation
4. Review the Legionella longbeachae trawling questionnaire.
5. HPS should consider a proposal for an in-depth epidemiological study of L. longbeachae
cases, to further investigate activities and high risk behaviours in such cases.
6. This cluster has highlighted differential use of PCR to detect Legionella in diagnostic
laboratories in Scotland. Highlight this issue with the Scottish Microbiology and Virology
Network and propose solutions that ensure provision of appropriate local and national
diagnostic tests for timely screening of samples from all regions in Scotland.
7. SHLMPRL should highlight the use of serology for the detection of non-pneumophila Sg1
strains of Legionella and issue a reminder of the availability of this service at SHLMPRL
to relevant diagnostic laboratory colleagues.
8. HPS should promote environmental research to further understand factors that affect
growth of L. longbeachae organism in growing media to a level which can cause illness.
29. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 25
Risk management
9. HPS should pursue the previous recommendations on improved surveillance and
exploration of novel approaches to awareness raising among at risk groups, and,
maintain an active dialogue with Scottish Government and Department of Health
regarding the issue of placing specific warning labels on bagged growing media.
30. 26 Cluster of Legionella longbeachae cases in Scotland in September/October 2013
8. References
1. Management of Public Health Incidents: Guidance on the Roles and Responsibilities of
NHS led Incident Management Teams, published by Scottish Government and HPN,
October 2011. Available at: http://www.scotland.gov.uk/Publications/2012/04/7816/
downloads#res392131
2. Public Health (Scotland) Act 2008, available at: http://www.scotland.gov.uk/
Resource/0039/00398162.pdf
3. European Centre for Disease Control, website available at: http://ecdc.europa.eu/en/Pages/
home.aspx
4. European Legionnaires’ Disease Surveillance Network (ELDSNet), web pages available at:
http://ecdc.europa.eu/en/activities/surveillance/ELDSNet/Pages/index.aspx
5. Guideline on the management of Legionella incidents, outbreaks and clusters in the
community, published HPN, March 2009, available at: http://www.hps.scot.nhs.uk/resp/
guidelinedetail.aspx?id=38930subjectid=185,97
6. Details of Legionnaires’ disease in Scotland available from HPS website at: http://www.hps.
scot.nhs.uk/resp/Legionella.aspx?subjectid=185,97
7. Legionellosis in Scotland in 2011 and 2012, published by HPS, August 2013, available at:
http://www.hps.scot.nhs.uk/resp/wrdetail.aspx?id=55879
8. Legionnaires’ disease in Europe in 2011, published by ECDC, April 2013, available at: http://
ecdc.europa.eu/en/publications/Publications/legionnaires-disease-in-europe-2011.pdf
9. Whiley H and Bentham R. Legionella longbeachae and legionellosis. Emerging Infectious
Diseases, 2011, 17, 4, 579.
10. Steele TW, Moore CV and Sangster N. Distribution of Legionella longbeachae Serogroup
1 and other Legionellae in potting soils in Australia. Applied Environmental Microbiology,
1990, 56, 10, 2984-2988.
11. Currie SL, Beattie TL, Knapp CW and Lindsay DSJ. Legionella spp. in UK composts - a
potential public health issue? Clinical Microbiology Infection, 2013, first published online
24 Oct 2013
12. Increased incidence of Legionnaires’ disease caused by Legionella longbeachae in Scotland:
Report from a National Incident Management Team, published by HPS, September 2013,
available at: http://www.hps.scot.nhs.uk/resp/publicationsdetail.aspx?id=56005
13. DEFRA white paper setting out aims to reduce peat in growing media in the UK, available
at: http://www.defra.gov.uk/environment/natural/whitepaper/
14. O’Connor BA, Carman J, Echert K, Tucker G, Givney R and Cameron S. Does potting mix
make you sick? Results from a Legionella longbeachae case-control study in South Australia.
Epidemiol. Infect., 2007, 135, 34-39.
15. PAS100 standard, details available from WRAP website: http://www.wrap.org.uk/content/
bsi-pas-100-producing-quality-compost
16. Association for Organics Recycling (AfOR) L. longbeachae guidance, available at: http://www.
organics-recycling.org.uk/uploads/article1894/39_AfOR_guidance_Legionella_longbeachae_
I1R0.pdf
31. Cluster of Legionella longbeachae cases in Scotland in September/October 2013 27
9. Appendices
9.1 Members of the national IMT
Martin Donaghy Chair of IMT,
Consultant in Public Health Medicine Health Protection Scotland
Alison Potts Epidemiologist Health Protection Scotland
Kevin Pollock Epidemiologist Health Protection Scotland
Michelle Marley Environmental Health Advisor Health Protection Scotland
Lynn Kidd Communications National Services Scotland
Joyce Dalgleish Communications National Services Scotland
Richard Othieno Consultant in Public Health Medicine NHS Lothian
Janet Stevenson Consultant in Public Health Medicine NHS Lothian
Lorna Willocks Consultant in Public Health Medicine NHS Lothian
Peter Harrison Health Protection Nurse NHS Lothian
David Ridd Communications NHS Lothian
Kirsty Licence Consultant in Public Health Medicine NHS Tayside
Jackie Hyland Consultant in Public Health Medicine NHS Tayside
Giles Edwards Consultant Microbiologist SHLMPRL
Diane Lindsay Senior Clinical Scientist SHLMPRL
Mary Hanson Consultant Microbiologist NHS Lothian
Kristjan Helgason Consultant Microbiologist NHS Lothian
Michael Lockhart Consultant Microbiologist NHS Tayside
Robbie Beattie Senior Manager/Public Analyst City of Edinburgh Council
Scientific Services
Iain McCluskey EHO West Lothian Council
Calum Sharp EHO City of Edinburgh Council
Carly Smith EHO City of Edinburgh Council
Margaret Gregory Senior EHO Angus Council
Malcolm Elliot EHO East Lothian Council
Duncan McCormick Senior Medical Officer Scottish Government
Simon Cuthbert-Kerr Policy Advisor Scottish Government
Nick Phin Consultant Epidemiologist Public Health England
Linda Moan Minute taker, Project Support Officer Health Protection Scotland
32. Health Protection Scotland, NHS National Services Scotland,
Meridian Court, 5 Cadogan Street,
Glasgow G2 6QE