Legionnaires' disease caused by Legionella ...

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IJID 1821 1–3 International Journal of Infectious Diseases xxx (2013) e1–e3

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Short Communication

Legionnaires’ disease caused by Legionella longbeachae in Taiwan, 2006–2010§ Wei a,b, Lei-Ron Tseng a, Jei-Kai Tan a, Chin-Yu Cheng a, Yen-Tao Hsu b,c, En-Tsung Cheng d, Chia-Sheng Lu e, Yao-Chuan Hsiao f, Tsai-Hung Wu g,h, Jui-Feng Hsu i, Ming-Tsan Liu a, Jung-Jung Mu a, Wan-Chin Chen a, Tsung-Pei Tsou a, Min-Nan Hung a, Chuen-Sheue Chiang a,j,*

Q1 Sung-Hsi

a

Center for Research, Diagnostics, and Vaccine Development, Centers for Disease Control, No. 161, Kun-Yang Street, Taipei, Taiwan Institute of Public Health, National Yang-Ming University, Taipei, Taiwan Department of Internal Medicine, Heping Fuyou Branch, Taipei City Hospital, Taipei, Taiwan d Department of Internal Medicine, Show-Chwan Memorial Hospital, Changhua, Taiwan e Department of Internal Medicine, En Chu Kong Hospital, Taipei, Taiwan f Department of Internal Medicine, Changhua Christian Hospital, Changhua, Taiwan g Department of Internal Medicine, Taipei Veterans General Hospital, Taipei, Taiwan h Department of Medicine, National Yang-Ming University, Taipei, Taiwan i Department of Internal Medicine, Kaohsiung Municipal Ta-Tung Hospital, Kaohsiung, Taiwan j Center of General Education, National Taipei University of Nursing and Health Sciences, Taipei, Taiwan b c

A R T I C L E I N F O

S U M M A R Y

Article history: Received 6 August 2013 Received in revised form 4 October 2013 Accepted 5 October 2013

The aim of the present study was to investigate the epidemiology of Legionnaires’ disease (LD) caused by Legionella longbeachae in Taiwan during 2006–2010. A total of six cases were identified prospectively, accounting for 1.6% of all laboratory-confirmed LD cases and 4.4% of culture-positive LD cases. All six cases occurred between April and August. The male to female ratio was 0.5. These six LD patients had a higher median age than those with LD due to Legionella pneumophila. Four of the six patients presented with pleural effusion and five survived the infection episode. Only two patients had a potential soil contact history prior to LD onset. The patients resided in divergent geographical areas without a common exposure history. The individual genomic DNA banding patterns of the six L. longbeachae isolates analyzed by pulsed-field gel electrophoresis (PFGE) were unique, supporting the hypothesis that the L. longbeachae infections occurred sporadically. ß 2013 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. All rights reserved.

Corresponding Editor: Eskild Petersen, Aarhus, Denmark Keywords: Legionnaires’ disease Legionella longbeachae Taiwan

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1. Introduction

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Legionnaires’ disease (LD) is a bacterial infection characterized by pneumonia. The majority of LD cases are caused by Legionella pneumophila, especially serogroup 1, but many Legionella species are pathogenic for humans.1–3 In Europe and the USA, L. pneumophila accounts for more than 90% of LD cases, while Legionella longbeachae accounts for less than 5%.1,4 In contrast, L. longbeachae is one of the leading causes of LD in Australia and New

§ This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited. * Corresponding author. Tel.: +886 (2) 26531350; fax: +886 (2) 27885075. E-mail address: [email protected] (C.-S. Chiang).

Zealand.3,5,6 Here, we report the epidemiology of LD caused by L. longbeachae in Taiwan for the first time.

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2. Methods

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LD has been a notifiable disease in Taiwan since 1999. It is mandatory for hospitals to report suspected cases within 7 days of diagnosis and to deliver clinical specimens to the Centers for Disease Control in Taiwan (TCDC) for laboratory diagnosis. Besides a clinical presentation of pneumonia, a confirmed diagnosis of LD is based on isolation of Legionella from respiratory secretions, detection of L. pneumophila serogroup 1 antigen in urine, or demonstration of a four-fold or greater rise in the antibody titer to at least 128 against L. pneumophila serogroup 1 to 6 between paired acute- and convalescent-phase sera. Species and serotypes of Legionella isolates are determined by specific antibodies (m-TECH/ Monoclonal Technologies, Inc., Atlanta, GA, USA).

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1201-9712/$36.00 – see front matter ß 2013 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. All rights reserved. http://dx.doi.org/10.1016/j.ijid.2013.10.004

Please cite this article in press as: Wei S-H, et al. Legionnaires’ disease caused by Legionella longbeachae in Taiwan, 2006–2010. Int J Infect Dis (2013), http://dx.doi.org/10.1016/j.ijid.2013.10.004

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IJID 1821 1–3 S.-H. Wei et al. / International Journal of Infectious Diseases xxx (2013) e1–e3

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Table 1 Demographic information, underlying diseases, soil contact history within 10 days prior to Legionnaires’ disease onset, and disease outcome for patients with disease caused by Legionella longbeachae in Taiwan, 2006–2010. Patient No.

Disease onset

Age/ gender

Residence

Underlying disease

Smoking

Soil contact history

Pleural effusion

Intensive care

Mechanical ventilator

Outcome

1 2 3

2006 Jun 2006 Aug 2007 Apr

90/F 72/F 75/F

Northern Taiwan Central Taiwan Northern Taiwan

Osteoarthritis Liver cirrhosis End-stage renal disease

No No No

Yes No No

Yes Yes Yes

Yes Yes Yes

Died Cured Cured

4

2010 Jul

80/F

Central Taiwan

Non-Hodgkin lymphoma, diabetes mellitus

No

Yes

Yes

Yes

Cured

5

2010 Jul

32/M

Northern Taiwan

Yes

Yes

Yes

No

Cured

6

2010 Aug

59/M

Southern Taiwan

Chronic kidney disease, gout Hypertension

No No Tomb-sweeping activity Growing vegetables with commercial compost No

No

No

Yes

Yes

Yes

Cured

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3. Results

4. Discussion

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The first LD case caused by L. longbeachae in Taiwan was identified in 2006, followed by five additional cases up until 2010. During this period, a total of 365 LD cases were laboratoryconfirmed and 137 of these (37.5%) were culture-positive for Legionella, including 114 L. pneumophila serogroup 1, 13 L. pneumophila non-serogroup 1, six L. longbeachae serogroup 1, and four other species. Therefore, L. longbeachae accounted for 1.6% of all laboratory-confirmed LD cases and 4.4% of culture-positive LD cases. Of the 137 culture-positive LD patients, those with disease caused by L. longbeachae had a higher median age than those with disease due to L. pneumophila, although the difference was not statistically significant (73.5 (range 32–90) years old vs. 67 (range 24–92) years old). The male to female ratio of LD patients with disease caused by L. longbeachae was significantly lower than that of patients with disease caused by L. pneumophila (0.5 vs. 4.8, p = 0.012, Fisher’s exact test). The demographic information, underlying diseases, soil contact history prior to LD onset, and disease outcome for the six patients are presented in Table 1. The patients resided in different geographical areas, did not know each other, and had no common contact or exposure history. The genomic DNA banding pattern of each L. longbeachae isolate analyzed by pulsed-field gel electrophoresis (PFGE) was unique (Figure 1), supporting the hypothesis that the L. longbeachae infections occurred sporadically.

In our study, only 4.4% of culture-positive LD was caused by L. longbeachae, while 92.7% was due to L. pneumophila. This large difference in prevalence is similar to that reported in Europe and the USA,1,4 but different from that in Australia and New Zealand.3,5,6 All six LD cases caused by L. longbeachae in our study occurred between April and August, similar to the situation in New Zealand,5 where the incidence of LD due to L. longbeachae peaks in the spring and summer months during which most gardening activities take place. In contrast, the incidence peaks between September and December in Thailand.7 The median age of LD patients with disease caused by L. longbeachae was higher than that of patients with disease due to L. pneumophila in our study, consistent with the observation of Amodeo et al. (73.2 vs. 59.3 years old).5 However, the male to female ratio of LD patients with disease caused by L. longbeachae in our study was much lower than previously reported values, which range from 1.6 to 4.9.5,7,8 Two patients (33.3%) in our study had a potential soil contact history within 10 days prior to LD onset: vegetable growing and tomb-sweeping. The tomb-sweeping activity is a major tradition for Chinese, during which people weed their ancestors’ tombs and thus might be exposed to soil. Since no soil samples were available for examination of Legionella, we were unable to relate these cases to sources of L. longbeachae. However, the low prevalence of soil contact history among our cases is not compatible with previous observations on the sources of L. longbeachae infection,6,9 suggesting that other sources of L. longbeachae infection might exist in Taiwan. In our study, four patients (66.7%) presented with pleural effusion and all six patients required intensive care (ICU stay 5–44 days). Amodeo et al. reported that 8% of LD patients with disease caused by L. longbeachae presented with pleural effusion and 42% of patients were treated in the ICU setting.5 For the diagnosis of L. longbeachae infection, culture of respiratory specimens is the only reliable method. This method is not carried out routinely for community-acquired pneumonia in Taiwan. Therefore, patients who are hospitalized with a severe L. longbeachae infection are more likely to be reported to the TCDC, probably contributing, at least in part, to the apparent difference in disease severity.

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Acknowledgements

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We thank Dr Daniela Schmid from the Austrian National Reference Centre for Legionella Infection, Austrian Agency for Health and Food Safety, Vienna, Austria, for comments on the manuscript. This work was supported by grants DOH98-DC-2004, DOH99-DC-2007, DOH100-DC-2015, DOH100-DC-2019, DOH101DC-2202, DOH102-DC-2502, and DOH102-DC-2601 from the Centers for Disease Control, Ministry of Health and Welfare, Taiwan.

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Figure 1. PFGE patterns for Legionella longbeachae isolates from Legionnaires’ disease patients. Genomic DNA was digested with SfiI and separated in 1% agarose gel by Bio-Rad CHEF MAPPER. Lane M, reference size maker (XbaI-digested genomic DNA fragments of Salmonella enterica ser. Braenderup H9812); lanes 1–6, patient isolates 1–6, respectively.


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Funding source: The study sponsor played no role in the study design, in the collection, analysis and interpretation of data, in the writing of the manuscript, or in the decision to submit the manuscript for publication. Conflict of interest: No conflict of interest to declare.

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