Legionnaire's disease, weather and climate

Ryota Sakamoto About the author

In the summer of 1976, at a convention for the American Legion, a mysterious outbreak of pneumonia affected 182 people, of whom 29 died. The spread of the infection appeared to be airborne, but it was not until the following year that the cause was identified as a bacterium. Legionnaire's disease, as it is now known, is caused by inhalation of aerosols (fine particles or droplets), containing bacteria of the genus Legionella. This pattern of transmission means that the disease is likely to be affected by weather and climate, but the Intergovernmental Panel on Climate Change, (IPCC) did not include it in its recent report.1. Climate change 2014: impacts, adaptation, and vulnerability. Geneva: Intergovernmental Panel on Climate Change; 2014. This paper argues that Legionnaire's disease should now be added to the IPCC's list of important climate-sensitive health issues.

Legionella accounts for 2-15% of hospital admissions for community-acquired pneumonia, with a summer or autumn peak in incidence. Although Legionella seems be detected throughout the world, in many countries relevant laboratory tests are unavailable and the incidence of legionellosis is not known. According to population-based surveillance conducted in Ohio, United States of America, in 1997, the annual number of cases of legionellosis requiring hospitalization was estimated at 7 per 100 000 population.2. Marston BJ, Plouffe JF, File TM Jr, Hackman BA, Salstrom SJ, Lipman HB, et al. The Community-Based Pneumonia Incidence Study Group. Incidence of community-acquired pneumonia requiring hospitalization. Results of a population-based active surveillance study in Ohio. Arch Intern Med. 1997 Aug 11-25;157(15):1709-18. http://dx.doi.org/10.1001/archinte.1997.00440360129015 PMID:9250232
http://dx.doi.org/10.1001/archinte.1997....
This incidence cannot, however, be generalized to other areas because transmission will be affected by local conditions.

Legionella is ubiquitous in the natural environment, especially in damp soil and water.3. Sakamoto R, Ohno A, Nakahara T, Satomura K, Iwanaga S, Kouyama Y, et al. Legionella pneumophila in rainwater on roads. Emerg Infect Dis. 2009 Aug;15(8):1295-7. http://dx.doi.org/10.3201/eid1508.090317 PMID:19751596
http://dx.doi.org/10.3201/eid1508.090317...
8. van Heijnsbergen E, Schalk JAC, Euser S, Brandsema PS, den Boer JW, De Roda Husman AM. Confirmed and potential sources of Legionella reviewed. Environ Sci Technol. 2015 Mar 16;150316110824006. http://dx.doi.org/10.1021/acs.est.5b00142 PMID:25774976
http://dx.doi.org/10.1021/acs.est.5b0014...
Given that the organism is present more or less everywhere, what factors are responsible for occurrence of the disease - and are the same pathways responsible for both outbreaks and sporadic cases? Legionella is an intracellular parasite that multiplies inside host cells. In the natural environment, these cells include aquatic protozoa, and in humans, macrophages. When exposed to unsuitable conditions, (i.e. too cold or too dry) Legionella alters its metabolism and remains viable but not culturable. Water temperatures of 25-42 °C are ideal conditions for rapid growth.7. Falkinham JO 3rd, Hilborn ED, Arduino MJ, Pruden A, Edwards MA. Epidemiology and ecology of opportunistic premise plumbing pathogens: Legionella pneumophila, Mycobacterium avium, and Pseudomonas aeruginosa. Environ Health Perspect. 2015 Mar 20; http://dx.doi.org/10.1289/ehp.1408692 PMID:25793551
http://dx.doi.org/10.1289/ehp.1408692...
This explains why outbreaks of Legionnaire's disease have often been linked to contaminated artificial water systems - especially air conditioning units in large buildings which use water for cooling.

Studies of associations between weather variables and sporadic cases of legionellosis suggest alternative potential exposure pathways. Associations have been reported between legionellosis and several weather variables,9. Fisman DN, Lim S, Wellenius GA, Johnson C, Britz P, Gaskins M, et al. It's not the heat, it's the humidity: wet weather increases legionellosis risk in the greater Philadelphia metropolitan area. J Infect Dis. 2005 Dec 15;192(12):2066-73. http://dx.doi.org/10.1086/498248 PMID:16288369
http://dx.doi.org/10.1086/498248...
1515 . Dunn CE, Rowlingson B, Bhopal RS, Diggle P. Meteorological conditions and incidence of Legionnaires' disease in Glasgow, Scotland: application of statistical modelling. Epidemiol Infect. 2013 Apr;141(4):687-96. http://dx.doi.org/10.1017/S095026881200101X PMID:22687530
http://dx.doi.org/10.1017/S0950268812001...
but the most consistent results relate to rainfall. Fisman et al. found that legionellosis was associated with rainfall 6-10 days before disease onset.9. Fisman DN, Lim S, Wellenius GA, Johnson C, Britz P, Gaskins M, et al. It's not the heat, it's the humidity: wet weather increases legionellosis risk in the greater Philadelphia metropolitan area. J Infect Dis. 2005 Dec 15;192(12):2066-73. http://dx.doi.org/10.1086/498248 PMID:16288369
http://dx.doi.org/10.1086/498248...
This timing corresponds to the latent period between exposure to the pathogen and the development of symptoms. Several subsequent studies have identified small but statistically significant increases in the risk of legionellosis with increased rainfall after a lag time of one to two weeks.1010 . Hicks LA, Rose CE Jr, Fields BS, Drees ML, Engel JP, Jenkins PR, et al. Increased rainfall is associated with increased risk for legionellosis. Epidemiol Infect. 2007 Jul;135(5):811-7. http://dx.doi.org/10.1017/S0950268806007552 PMID:17121693
http://dx.doi.org/10.1017/S0950268806007...
1111 . Garcia-Vidal C, Labori M, Viasus D, Simonetti A, Garcia-Somoza D, Dorca J, et al. Rainfall is a risk factor for sporadic cases of Legionella pneumophila pneumonia. PLoS ONE. 2013;8(4):e61036. http://dx.doi.org/10.1371/journal.pone.0061036 PMID:23613778
http://dx.doi.org/10.1371/journal.pone.0...
1313 . Chen NT, Chen MJ, Guo CY, Chen KT, Su HJ. Precipitation increases the occurrence of sporadic legionnaires' disease in Taiwan. PLoS ONE. 2014;9(12):e114337. http://dx.doi.org/10.1371/journal.pone.0114337 PMID:25474539
http://dx.doi.org/10.1371/journal.pone.0...
1414 . Halsby KD, Joseph CA, Lee JV, Wilkinson P. The relationship between meteorological variables and sporadic cases of Legionnaires' disease in residents of England and Wales. Epidemiol Infect. 2014 Nov;142(11):2352-9. http://dx.doi.org/10.1017/S0950268813003294 PMID:24406306
http://dx.doi.org/10.1017/S0950268813003...

It is plausible that rainfall might affect exposure to Legionella, via a range of potential mechanisms. Contamination of reticulated drinking water is a possibility,7. Falkinham JO 3rd, Hilborn ED, Arduino MJ, Pruden A, Edwards MA. Epidemiology and ecology of opportunistic premise plumbing pathogens: Legionella pneumophila, Mycobacterium avium, and Pseudomonas aeruginosa. Environ Health Perspect. 2015 Mar 20; http://dx.doi.org/10.1289/ehp.1408692 PMID:25793551
http://dx.doi.org/10.1289/ehp.1408692...
but a one or two week lag time seems too short for this pathway. Another suggestion is that vehicles might produce aerosols containing Legionella, as they drive on wet road surfaces.3. Sakamoto R, Ohno A, Nakahara T, Satomura K, Iwanaga S, Kouyama Y, et al. Legionella pneumophila in rainwater on roads. Emerg Infect Dis. 2009 Aug;15(8):1295-7. http://dx.doi.org/10.3201/eid1508.090317 PMID:19751596
http://dx.doi.org/10.3201/eid1508.090317...
1313 . Chen NT, Chen MJ, Guo CY, Chen KT, Su HJ. Precipitation increases the occurrence of sporadic legionnaires' disease in Taiwan. PLoS ONE. 2014;9(12):e114337. http://dx.doi.org/10.1371/journal.pone.0114337 PMID:25474539
http://dx.doi.org/10.1371/journal.pone.0...
Molecular matching of clinical and environmental samples is a promising approach that provides some support for this hypothesis.4. Kanatani J, Isobe J, Kimata K, Shima T, Shimizu M, Kura F, et al. Close genetic relationship between Legionella pneumophila serogroup 1 isolates from sputum specimens and puddles on roads, as determined by sequence-based typing. Appl Environ Microbiol. 2013 Jul;79(13):3959-66. http://dx.doi.org/10.1128/AEM.00637-13 PMID:23603681
http://dx.doi.org/10.1128/AEM.00637-13...

The environmental sources and global impact of legionellosis should now be reassessed. Being aware that Legionella is ubiquitous is not sufficient. It exists in the environment surrounding us, but which sources are the most important for human health? According to the IPCC, increases in heavy rainfall are projected as a result of global climate change.1616 . Climate change 2013: the physical science basis. Geneva: Intergovernmental Panel on Climate Change; 2013. Climate change might increase the incidence of legionellosis through increased reliance on air conditioning systems, as well as through more subtle effects on bacterial ecology or airborne exposure pathways.

References

  • 1
    Climate change 2014: impacts, adaptation, and vulnerability. Geneva: Intergovernmental Panel on Climate Change; 2014.
  • 2
    Marston BJ, Plouffe JF, File TM Jr, Hackman BA, Salstrom SJ, Lipman HB, et al. The Community-Based Pneumonia Incidence Study Group. Incidence of community-acquired pneumonia requiring hospitalization. Results of a population-based active surveillance study in Ohio. Arch Intern Med. 1997 Aug 11-25;157(15):1709-18. http://dx.doi.org/10.1001/archinte.1997.00440360129015 PMID:9250232
    » http://dx.doi.org/10.1001/archinte.1997.00440360129015
  • 3
    Sakamoto R, Ohno A, Nakahara T, Satomura K, Iwanaga S, Kouyama Y, et al. Legionella pneumophila in rainwater on roads. Emerg Infect Dis. 2009 Aug;15(8):1295-7. http://dx.doi.org/10.3201/eid1508.090317 PMID:19751596
    » http://dx.doi.org/10.3201/eid1508.090317
  • 4
    Kanatani J, Isobe J, Kimata K, Shima T, Shimizu M, Kura F, et al. Close genetic relationship between Legionella pneumophila serogroup 1 isolates from sputum specimens and puddles on roads, as determined by sequence-based typing. Appl Environ Microbiol. 2013 Jul;79(13):3959-66. http://dx.doi.org/10.1128/AEM.00637-13 PMID:23603681
    » http://dx.doi.org/10.1128/AEM.00637-13
  • 5
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    » http://dx.doi.org/10.1007/s00284-008-9192-y
  • 7
    Falkinham JO 3rd, Hilborn ED, Arduino MJ, Pruden A, Edwards MA. Epidemiology and ecology of opportunistic premise plumbing pathogens: Legionella pneumophila, Mycobacterium avium, and Pseudomonas aeruginosa. Environ Health Perspect. 2015 Mar 20; http://dx.doi.org/10.1289/ehp.1408692 PMID:25793551
    » http://dx.doi.org/10.1289/ehp.1408692
  • 8
    van Heijnsbergen E, Schalk JAC, Euser S, Brandsema PS, den Boer JW, De Roda Husman AM. Confirmed and potential sources of Legionella reviewed. Environ Sci Technol. 2015 Mar 16;150316110824006. http://dx.doi.org/10.1021/acs.est.5b00142 PMID:25774976
    » http://dx.doi.org/10.1021/acs.est.5b00142
  • 9
    Fisman DN, Lim S, Wellenius GA, Johnson C, Britz P, Gaskins M, et al. It's not the heat, it's the humidity: wet weather increases legionellosis risk in the greater Philadelphia metropolitan area. J Infect Dis. 2005 Dec 15;192(12):2066-73. http://dx.doi.org/10.1086/498248 PMID:16288369
    » http://dx.doi.org/10.1086/498248
  • 10
    Hicks LA, Rose CE Jr, Fields BS, Drees ML, Engel JP, Jenkins PR, et al. Increased rainfall is associated with increased risk for legionellosis. Epidemiol Infect. 2007 Jul;135(5):811-7. http://dx.doi.org/10.1017/S0950268806007552 PMID:17121693
    » http://dx.doi.org/10.1017/S0950268806007552
  • 11
    Garcia-Vidal C, Labori M, Viasus D, Simonetti A, Garcia-Somoza D, Dorca J, et al. Rainfall is a risk factor for sporadic cases of Legionella pneumophila pneumonia. PLoS ONE. 2013;8(4):e61036. http://dx.doi.org/10.1371/journal.pone.0061036 PMID:23613778
    » http://dx.doi.org/10.1371/journal.pone.0061036
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    Conza L, Casati S, Limoni C, Gaia V. Meteorological factors and risk of community-acquired Legionnaires' disease in Switzerland: an epidemiological study. BMJ Open. 2013;3(3):e002428. http://dx.doi.org/10.1136/bmjopen-2012-002428 PMID:23468470
    » http://dx.doi.org/10.1136/bmjopen-2012-002428
  • 13
    Chen NT, Chen MJ, Guo CY, Chen KT, Su HJ. Precipitation increases the occurrence of sporadic legionnaires' disease in Taiwan. PLoS ONE. 2014;9(12):e114337. http://dx.doi.org/10.1371/journal.pone.0114337 PMID:25474539
    » http://dx.doi.org/10.1371/journal.pone.0114337
  • 14
    Halsby KD, Joseph CA, Lee JV, Wilkinson P. The relationship between meteorological variables and sporadic cases of Legionnaires' disease in residents of England and Wales. Epidemiol Infect. 2014 Nov;142(11):2352-9. http://dx.doi.org/10.1017/S0950268813003294 PMID:24406306
    » http://dx.doi.org/10.1017/S0950268813003294
  • 15
    Dunn CE, Rowlingson B, Bhopal RS, Diggle P. Meteorological conditions and incidence of Legionnaires' disease in Glasgow, Scotland: application of statistical modelling. Epidemiol Infect. 2013 Apr;141(4):687-96. http://dx.doi.org/10.1017/S095026881200101X PMID:22687530
    » http://dx.doi.org/10.1017/S095026881200101X
  • 16
    Climate change 2013: the physical science basis. Geneva: Intergovernmental Panel on Climate Change; 2013.

Publication Dates

  • Publication in this collection
    June 2015

History

  • Received
    06 Feb 2014
  • Reviewed
    22 Jan 2015
  • Accepted
    23 Jan 2015
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