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Respiratory Infections

28 August 2013

Legionellosis in Scotland in 2011 and 2012

1 Introduction

1.1 Description of disease

Legionellosis is associated with two clinically and epidemiologically distinct illnesses:

  • Legionnaires' disease (characterised by pneumonia and fever, myalgia, cough); and
  • Pontiac fever (a milder flu-like illness without pneumonia).

Legionnaires' disease is an uncommon and potentially fatal form of pneumonia caused by Legionella bacteria. Legionella bacteria are distributed widely in both natural and artificial water supplies and in soil. In most cases, disease is caused by the inhalation of aerosolised water containing Legionella bacteria. Sources include showers, air conditioning, cooling towers, humidifiers, whirlpool spas and fountains.

Legionella bacteria are fastidious gram-negative rods. They grow best in warm water (25-45ºC), but have been found to survive in temperatures ranging from 6oC to 60oC. They prefer water which is stagnant and are associated with bio-films and amoebae.

The majority of cases of Legionnaires' disease are caused by Legionella pneumophila. There are 16 recognised serogroups of L. pneumophila, of which serogroup 1 (Sg1) is the most common, causing more than 80% of cases of Legionnaires' disease.1 In addition there are over 50 other species of Legionella, more than 20 of which have been shown to cause human disease. There is evidence of previous exposure to Legionella species in a high proportion of the population, as determined in seroprevalence studies in blood-donor blood. However, evidence of previous exposure to L. pneumophila Sg1 is more uncommon.

The incidence of Legionnaires' disease in Scotland is low and there are usually between 20 and 40 cases per year, the majority of which are contracted overseas. Older age and male gender are both associated with increased risk, as is smoking and underlying respiratory disease.

1.2 Legionellosis surveillance in Scotland

Health Protection Scotland (HPS) has undertaken enhanced surveillance of Legionella infections in conjunction with the Scottish Haemophilus Legionella Meningococcus Pneumococcus Reference Laboratory (SHLMPRL) since 1994. The purpose of this enhanced surveillance is to characterise the Legionella species causing illness, identify the likely source of infection and inform measures to reduce the public health risk. This involves characterising, identifying and monitoring trends. Surveillance in Scotland is integrated with the rest of the UK and with Europe.

The majority of cases of Legionnaires' disease are admitted to hospital and the disease is detected during tests run whilst in hospital. Cases of Pontiac fever are not usually detected unless they are part of an outbreak when awareness amongst primary care staff and potential cases is raised. Patient samples are tested locally, but are normally confirmed as positive by re-testing at the reference laboratory. Once cases are confirmed, the NHS board where the patient has been residing will undertake an investigation which aims to define any risks for exposure and to put in place any control measures to prevent others being exposed. The NHS board is requested to complete an enhanced surveillance report form and return it to HPS. This collects demographic data, information on the clinical presentation and risk factors for each patient, and detailed information on travel away from home during the incubation period of the illness (2-10 days prior to onset of symptoms). All cases suspected to be travel-related are immediately reported to the European Legionnaires' Disease Surveillance Network (ELDSNet), which aims to quickly identify clusters of cases across Europe and prompt source identification.

HPS publishes summaries every two years of legionellosis in Scotland. Readers are referred to previous reports for more detailed information about past years.2 This report provides an update on cases of legionellosis in Scotland between January 2011 and December 2012.

Under Scottish Government / Health Protection Network guidance on the Management of Public Health Incidents,3 NHS boards should notify HPS of the occurrence of actual or potential Legionnaires' disease cases. Management of outbreaks which affect more than one NHS board is co-ordinated by HPS. This report provides a summary of those outbreaks reported to HPS in the period 2011-12.

1.3 Legionnaires' disease surveillance in Europe

Only the severe form of legionellosis, Legionnaires' disease, is monitored at a European level. This monitoring is administered by the European Centre for Disease Control (ECDC), through ELDSNet.4,5

Legionnaires' disease is monitored in two ways:

  1. annual submission of datasets of all Legionnaires' disease cases in member states;1,6,7
  2. immediate reporting of travel-related cases of Legionnaires' disease as they are diagnosed by member states.8 This aims to improve knowledge and information on the epidemiological and microbiological (both clinical and environmental) aspects of Legionnaires' disease, to locate sources of infection and to prevent further cases of infection.

In addition, ECDC member states are required to notify ECDC of outbreaks or other significant events which may present a risk to European citizens travelling to that country.

ECDC provides case definitions for Legionnaires' disease, which all member states use. In local outbreaks these definitions may be modified to be more inclusive, to allow more rapid identification of the infection source. For the purposes of routine surveillance and reporting to ECDC, HPS and SHLMPRL use the following definitions (taken from ECDC).9

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

  • isolation of Legionella species from respiratory secretions or any normally sterile site;
  • detection of Legionella pneumophila antigen in urine;
  • Legionella pneumophila serogroup 1 specific antibody response.

Probable cases of Legionnaires' disease must have clinically defined pneumonia and at least one of the following laboratory criteria:

  • detection of Legionella pneumophila antigen in respiratory secretions or lung tissue;
  • detection of Legionella species nucleic acid in a clinical specimen;
  • specific antibody response to Legionella pneumophila non-serogroup 1 or other Legionella species;
  • single high titre of specific antibody for Legionella pneumophila serogroup 1, other Legionella pneumophila serogroups or other Legionella species.

Cases are linked epidemiologically if at least one of the following criteria is met:

  • environmental exposure;
  • exposure to the same common source.

The case definition detailed above is the latest version available on the ELDSNet web pages, taken from the Commission Decision of 28 April 2008, when ECDC case definitions were reviewed and revised.9 This differs from the case definitions in the current Health Protection Network guidance,10 which incorporates the old ECDC case definitions. This update in definitions reflects changes to laboratory methods for detection of Legionella bacteria. HPS and SHLMPRL use the revised ECDC definitions for normal surveillance activities.

2 Descriptive Epidemiology

2.1 Characteristics of cases

The trend in the annual number of reference laboratory-confirmed cases of Legionnaires' disease diagnosed in Scotland between 2000 and 2012 is shown in Figure 1. In 2011 there were 32 cases, of which 28 were confirmed and four were probable cases (using the case definitions detailed in the section 1.3). In 2012 there were 104 cases of Legionnaires' disease, of which 81 were confirmed and 23 were probable. This unexpectedly high number includes 56 confirmed cases which were linked with an outbreak in south-west Edinburgh in May/June 2012. All of these cases reported in 2011 and 2012 were in Scottish residents.

In 2011 there were three cases of Legionnaires' disease in Scottish residents which were exposed, diagnosed and treated overseas. In 2012 there was one additional case of Legionnaires' disease in a Scottish resident, who was exposed, diagnosed and treated overseas. Data for those cases which were exposed, diagnosed and treated overseas are not included in this report.

2.2 Incidence

The annual incidence rate of Legionnaires' disease in Scotland was 6.0 cases per million population in 2011 and 19.6 cases per million in 2012. The incidence in 2011 continues the trend of relatively low incidence in Scotland when compared to the rest of Europe, which had an average incidence of 11.0 per million population in 2009,7 12.4 in 20107 and 9.7 in 2011.1 In 2012, the incidence in Scotland was much higher than the rate for Europe due to the outbreak in Edinburgh.

Cases of Legionnaires' disease were diagnosed in all quarters in 2011 and 2012. The highest numbers of cases were diagnosed in quarter 2 (April to June) and quarter 3 (July to September) in both years (Figure 2).. This is in line with patterns at a European level where the largest number of cases were diagnosed in June to September in 2011.1

2.3 Sex

Table 1 shows the breakdown by sex of cases in Scotland from 2000 to 2012. In 2011 72% of cases were male and in 2012 67% of cases were male. The general pattern of more cases in males than females is typical for Legionnaires' disease, with on average twice as many males cases in Scotland than female cases. In Europe in 2011, 71% of cases were male and 29% were female.1

2.4 Age

Legionnaires' disease is more common in older age groups. Figure 3 shows the age band distribution of cases in the years 2000-2012. In 2011, all cases were older than 40 years and in 2012 more than 94% of cases were older than 40 years. Across 2011 and 2012, the most common age range of cases was 60-69 years (52 cases, 38%).

2.5 Risk factors

Smoking and lung disease are known risk factors for legionellosis. For the case of Legionnaires' disease in 2011 and 2012, 61% were smokers, 31% did not smoke and for 8% of cases smoking status was not know or not recorded. This compares with 54% smokers in 2009-10 (27% did not smoke and 19% of cases smoking status was not known) and 44% smokers in 2007-08 (35% not smokers, 21% smoking status not known).

Immunocompromised individuals have increased risk of infection with a variety of pathogens. For cases of Legionnaires' disease in 2011 and 2012, 29% were immunocompromised, 64% were not immunocompromised and for 7% this was not known or not recorded. This compares with 20% immunocompromised in 2009-10 (75% not immunocompromised and 5% not known or not recorded) and 24% immunocompromised in 2007-08 (63% not immunocompromised and 13% not known or not recorded).

2.6 Clinical presentation

Epidemiological data presented in this report describes cases of Legionnaires' disease in 2011-12. In addition to these Legionnaires' disease cases some cases of Pontiac fever were reported to HPS. In 2011 there was one case of Pontiac fever linked to a cluster of Legionnaires' disease in holiday makers who visited Corfu, Greece and 156 cases of Pontiac fever linked to an outbreak of legionellosis in Tayside (see section 5.1 and 6.3.1). In 2012, cases of Pontiac fever were linked to the outbreak in Edinburgh (see section 5.4 and 6.3.3).

For cases of Legionnaires' disease, in 2011 91% cases presented with pneumonia and in 2012 98% cases presented with pneumonia. Other clinical symptoms for these cases included (in no particular order) fever, shortness of breath, dry cough, headache, muscle pain, lethargy, confusion, nausea, vomiting, diarrhoea, dizziness, shivers, thoracic pain, pleuritic pain, chest pain and collapse. It is not uncommon for cases of Legionnaires' disease to be admitted to intensive care facilities.

2.7 Mortality

There were six recorded deaths among cases of Legionnaires' disease reported in 2011 and six in 2012 (four of these were linked with the outbreak in Edinburgh) (Table 2). Mortality data captured through this surveillance scheme does not imply Legionella as the cause of death recorded on the death certificate.

For 2011 and 2012 the mean case fatality rate was 8.8%. This is similar to the rates seen in Scotland in previous years: 7.3% in 2009-10; 10.3% in 2007-08; 7.5% in 2004-06. The rate for 2011-12 remains below the European mean case fatality rate which was 10% in 2011 (which is similar to previous years). The small number of annual deaths in Scotland makes case fatality rates subject to large variation and therefore difficult to interpret.

3 Suspected settings for exposure to Legionella

Of the 136 cases reported in 2011 and 2012, 25% were travel-related; 73% were community-acquired; and 1% were hospital-acquired. This distribution is shown in Figure 4 and shows an increase in the number of community-acquired cases from the previous reporting period 2009-10 (66% travel related, 27% community-acquired; 2% hospital-acquired, 5% unknown origin). This increase in community acquired cases is principally due to the large outbreak in Edinburgh in 2012.

3.1 Travel-associated cases

The countries associated with travel-acquired cases are listed in Table 3. For 2011 and 2012 the majority of travel-related cases were associated with stays in accommodation sites within Europe - with travel to Spain, Greece, UK (including Scotland), Italy and Turkey accounting for the most travel-related cases.

In 2011, 10 cases were reported to ELDSNet, four cases have been attributed to clusters – these are defined as cases from different countries that are suspected as having contracted Legionnaires' disease from the same accommodation site in a two-year period. In 2012, of the 17 cases which were reported to ELDSNet, five cases were linked with four different clusters.

3.2 Community-acquired cases

Of the 100 community-acquired cases in 2011 and 2012, 56 confirmed cases were associated with the outbreak in Edinburgh in 2012. One case was associated with in an outbreak of legionellosis in Tayside in 2011. For the remaining non-outbreak cases, environmental investigations were undertaken but no source could be identified. Due to the widespread and ubiquitous environmental distribution of Legionella bacteria, a specific source for most sporadic cases of community-acquired disease is never identified.

3.3 Hospital-acquired cases

Only one case of suspected hospital-acquired legionellosis was reported in 2011-12. For this case investigation of possible exposure within hospital was undertaken, but no source could be identified.

4 Cases of Legionnaires' disease in travellers to Scotland

In 2011-12, ELDSNet received a report of one case of Legionnaires' disease in a visitor to Scotland, linked to a single accommodation site within Scotland. On the basis of this single notification this accommodation site was investigated by local environmental health officers and given a clean bill of health.

5 Outbreaks

During the period 2011-2012, four actual or potential outbreaks were notified to HPS. These were:

  1. Outbreak of legionellosis in Tayside;
  2. Cluster of cases in Glasgow/Lanarkshire;
  3. Cases of Legionella longbeachae occurring throughout Scotland;
  4. Outbreak of legionellosis in Edinburgh.

5.1 Legionellosis in Tayside

In 2011, NHS Tayside investigated an outbreak of legionellosis linked to a hotel. This outbreak resulted in one case of Legionnaires' disease and 156 cases of Pontiac fever in staff and visitors to the hotel. This outbreak was widely reported in the media.

5.2 Cluster of cases Glasgow/Lanarkshire

NHS Greater Glasgow & Clyde led an investigation into 11 cases of Legionnaires' disease which occurred over a two- month period in 2011. Cases all had links to the east-end of Glasgow/Lanarkshire region and the unusually high number of cases during this period prompted further investigation. There was no common strain of Legionella associated with all or a high proportion of the cases. Extensive environmental investigations did not identify a likely source. The incident management team concluded that there was no strong evidence of a common exposure, and that, although occurring during a short time period, the cases were probably not directly linked.

5.3 National investigation into cases of Legionella longbeachae

In 2012, following nine cases reported in Scotland over a five-year period, HPS undertook an investigation into cases of Legionella longbeachae, linked with plant growing media (potting compost) exposure. The group reviewed clinical, microbiological and environmental information to identify possible explanations as to why cases were being reported in Scotland but not elsewhere in the UK. Additional information was sought from Australia and New Zealand where many cases of Legionella longbeachae are reported every year. The group concluded that most likely this difference in ascertainment was due to microbiological services in Scotland tending to investigate this type of Legionella and therefore detecting it more so than the rest of the UK. No differences could be found in production and transport of growing media for public sale. National standards are in place to quality control composted material which is included in growing media.

5.4 Outbreak of legionellosis in Edinburgh

NHS Lothian led the management of an outbreak of Legionnaires' disease and associated cases of milder illness in May/June 2012.11 This outbreak resulted in 56 confirmed cases of Legionnaires' disease of whom four died. It is likely that exposure was as a result of outdoor air pollution, released close to the affected area in south-west Edinburgh. This outbreak was widely reported in the media. Health and Safety enforcing authorities are investigating the circumstances of the deaths under the direction of the Crown Office and Procurator Fiscal Service Health and Safety Division. NHS Lothian released an interim report on the outbreak in July 2013.12

6 SHLMPRL testing for Legionella in 2011 and 2012

A total of 3,501 specimens for the diagnosis of legionellosis were submitted to SHLMPRL in 2011, an increase of 30% on 2010. In 2012, 4,931 specimens were submitted, an increase of 41% on 2011, see Table 4. This increase in specimen numbers in both years is largely due to two large outbreaks occurring in Tayside and Lothian in 2011 and 2012 respectively.

As always, SHLMPRL would encourage all laboratories to send any positive samples for confirmation before reporting to local public health departments.

6.1 Characteristics of laboratory confirmed cases of Legionella infection

In 2011 and 2012, 108 (40%) of all positive samples were confirmed by urinary antigen test, 85 (31%) by PCR, 8 (3%) by sero-conversion, 29 (11%) by single high antibody titre and 42 (15%) by culture isolation (Table 5).

A total of 42 cultured isolates were obtained from human illness in 2011 and 2012, see Table 6. Of these, 40 were confirmed as L. pneumophila Sg 1, one as L. pneumophila Sg 3, one as L. pneumophila Sg 10 and one as L. longbeachae. The breakdown of L. pneumophila Sg 1 isolates by monoclonal subtype was Knoxville (26), Philadelphia (7), Benidorm (6) and Allentown/France (1), see Table 6.

Sequence-based typing (SBT) was performed on all L. pneumophila isolates. This technique amplifies seven genes to give a genotype profile. This can be used to match a patient isolate to a possible environmental source. The introduction of nested SBT has allowed for further characterisation of PCR positive/culture negative cases. Nested SBT was an invaluable technique in the outbreaks that occurred in 2011 and 2012.

6.2 Environmental samples

A total of 83 environmental cultures were received in 2011 and 48 in 2012. This compares with 168, 252, 90, 183 and 207 in years 2010, 2009, 2008, 2007 and 2006 respectively. The species, serotypes and subtypes are shown in Table 6.

L. anisa was the most common species confirmed with 34 of 131 (26%), followed by L. pneumophila Sg 4 with 23 of 131 (17.5%), L. pneumophila Sg 6 with 16 of 131 (12%) and L. pneumophila Sg 1 was also 16 of 131 (12%). L. pneumophila Sg 1 consisted of monoclonal subtypes OLDA with 8 of 16 (50%), Bellingham with 5 of 16 (31%) and Benidorm with 3 of 16 (19%). Of the other species, two were L. steelei which to our knowledge is the first environmental isolation of this species. L longbeachae also continues to appear in environmental samples with two isolates in 2011 which were associated with a case of L. longbeachae Legionnaires' disease.

SHLMPRL encourages all labs to send Legionella species for confirmation as the mip gene sequencing identifies all Legionella species and was used to identify the first isolation of L. steelei.

6.3 Laboratory investigations

6.3.1 Tayside, 2011

An outbreak of legionellosis in Tayside in March 2011 resulted in a full microbiological and epidemiological investigation. The outbreak consisted mostly of cases of Pontiac fever. Diagnosis of cases of Pontiac fever is normally difficult and tends to rely on a specific antibody response. In the past, the proportion of Pontiac fever cases with elevated antibodies to environmentally isolated Legionella species has varied between 30-85%. In Tayside, investigations showed that the antibody response in this particular outbreak was much lower than expected. However, on further testing with antibodies raised against the particular strain of L. pneumophila isolated from the suspected environmental source, 156 cases were identified. Laboratory testing identified one case of Legionnaires' disease and 21 confirmed, 37 probable and 97 possible cases of Pontiac fever.

6.3.2 Glasgow/Lanarkshire cluster, 2011

Eleven cases of Legionnaires' disease were identified in the Glasgow area between April and June 2011. Urinary antigen tests were performed on all cases and serum serology was performed where possible. Isolates of L. pneumophila Sg 1 were obtained in three cases with sequence-based typing showing three different SBT types. The infecting strain in a fourth case was identified by nested SBT. The presence of four different strains was considered to decrease the possibility of a single common source. A further three cases were positive by urinary antigen with a further case also likely to be L. pneumophila from a partial nested SBT results. Four cases gave unusual urinary antigen results, although three of these had other microbiological evidence of Legionella infection and may represent infection with non- L. pneumophila species.

6.3.3 Edinburgh, 2012

In the large outbreak in south west Edinburgh in 2012, positive cultures were obtained from 15 patients and the causative organism was identified as L. pneumophila Sg1, monoclonal subtype Knoxville, sequence-based type ST 191 (6,10,19,28,19,4,6). Urinary antigen detection was the main diagnostic tool applied during this outbreak. However, PCR and culture were also invaluable and any PCR positive, culture negative cases were further sub-typed by nested SBT. All culture positive samples were typed using Dresden monoclonal antibodies. Fifty-six cases were confirmed by urinary antigen and/or culture. Ten probable and twenty-six possible cases were identified by PCR, serology and/or clinical diagnosis of pneumonia and association with the outbreak area. To date the environmental source has not been identified by culture.

7 New and planned developments over the next two years

7.1 Guideline on the management of Legionella outbreaks and clusters

Scottish guidance on Legionella outbreak management was produced by the Health Protection Network in March 2009 and is available on the HPN website.10 This evidence-based guidance is aimed at professionals of the wider health protection community in Scotland, considering issues around initial management response; epidemiological investigations; environmental investigations; sampling; risk assessment; communication; reporting and control. This guidance was due for review in 2012 but, due to the outbreak in Edinburgh in 2012, this was postponed so that any lessons learned during this outbreak could be incorporated into the revised guidance. The guideline review process has now commenced and should be completed in 2014.

7.2 Laboratory developments – new detection techniques

An RT PCR assay for detection of Legionella in respiratory samples is currently being validated. Initial results show that it can identify L. pneumophila Sg 1 strains of L. pneumophila and it is hoped to incorporate a Legionella species specific component to ensure that SHLMPRL continue to identify Legionella infections other than those caused by L. pneumophila Sg 1.

7.3 Legionella longbeachae recommendations

HPS has written a report on the investigation undertaken into the recent cases of L. longbeachae in Scotland. This report is currently under review by key stakeholders. Following this review process, HPS plans to publish this report.

7.4 Recent epidemiological investigations

HPS, together with lead NHS boards, plans to ensure that scientific evidence from collaborations in outbreak situations is used to help prevent further similar outbreaks and to enhance knowledge. This will be achieved by publication of outbreak investigation findings in the scientific literature.

7.5 Epidemiological methods for outbreak investigation

HPS is in the process of introducing new epidemiological methods for surveillance and outbreak investigation. These include new software that can be adapted quickly to establish outbreak databases; revised and specialised surveillance forms; and participation in studies utilising modern technologies. Specifically for legionellosis outbreak investigation, HPS continues to collaborate with the Met Office for wind flow data and advice on plumes and dispersal, and the Emergency Response Unit in Public Health England for mathematical modelling, including cluster analysis and release windows.

Acknowledgements

The authors would like to thank the microbiologists, consultants in public health medicine, clinicians, nurses, public health teams and other staff who assist in the submission of samples to SHLMPRL and in the completion of surveillance forms.

References

  1. Legionnaires' disease in Europe in 2011, report by ECDC, published March 2013, available at: http://ecdc.europa.eu/en/press/news/Lists/News/ECDC_DispForm.aspx?List=32e43ee8%2De230%2D4424%2Da783%2D85742124029a&ID=875&RootFolder=%2Fen%2Fpress%2Fnews%2FLists%2FNews.
  2. HPS web pages on Legionella http://www.hps.scot.nhs.uk/resp/legionella.aspx?subjectid=185,97.
  3. Scottish Government and Health Protection Network guidance on Management of Public Health Incidents, published 2011, available at: http://www.scotland.gov.uk/Publications/2012/04/7816/downloads#res392132.
  4. ECDC web pages on legionellosis http://ecdc.europa.eu/en/healthtopics/legionnaires_disease/Pages/index.aspx.
  5. ELDSNet web pages on the ECDC website http://ecdc.europa.eu/en/activities/surveillance/ELDSNet/Pages/index.aspx.
  6. Legionnaires' disease in Europe in 2010, report by ECDC, published July 2012, available at: http://ecdc.europa.eu/en/press/news/Lists/News/ECDC_DispForm.aspx?List=32e43ee8%2De230%2D4424%2Da783%2D85742124029a&ID=684&RootFolder=%2Fen%2Fpress%2Fnews%2FLists%2FNews.
  7. Beaute J, Zucs P, de Jong B. Legionnaires' disease in Europe 2009-10. Eurosurveillance, 2013: 18(10):pii=20417.
  8. Beaute J, Zucs P, de Jong B. risk for travel-associated Legionnaires' disease in Europe, 2009. Emerging Infectious Diseases, 2012: 18: 1811-16.
  9. ECDC case definitions, available at: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2008:159:0046:01:EN:HTML.
  10. HPN website for Guideline on the management of Legionella incidents, outbreaks and clusters in the community, published 2009, available at: http://www.hps.scot.nhs.uk/about/publications.aspx.
  11. McCormick D, Thorn S Milne D, Evans C, Stevenson J et al. Public health response to an outbreak of Legionnaires' disease in Edinburgh, UK, June 2012. Eurosurveillance, 2012:17(28):pii=20216.
  12. Interim report into the Legionnaires' disease outbreak in Edinburgh 2012, NHS Lothian, published 2013, available at: http://www.nhslothian.scot.nhs.uk/MediaCentre/PressReleases/2013/Pages/Interim-report-into-Edinburgh-Legionnaires'-outbreak---.aspx.
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Author(s): Prepared by: Alison Potts, John Love, Katy Sinka, Kevin Pollock, Martin Donaghy, Diane Lindsay, Alistair Brown, and Giles Edwards Vol: 47 No: 35 Year: 2013 Page:

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