The role of air temperature in Legionella water contamination and legionellosis incidence rates in southern Italy (2018–2023)

The role of air temperature in Legionella water contamination and legionellosis incidence rates in southern Italy (2018–2023)

Authors

  • M. T. Montagna
  • S. Brigida
  • F. Fasano
  • C. M. Leone
  • M. D'Ambrosio
  • V. Spagnuolo
  • M. Lopuzzo
  • F. Apollonio
  • F. Triggiano
  • M. E. Caringella
  • O. De Gilgio

Keywords:

Legionnaires’ disease, Legionella pneumophila, air temperature, climate change, public health, waterborne disease

Abstract

Background. Legionnaires’ disease is caused by inhalation or aspiration of small water droplets contaminated with Legionella, commonly found in natural and man-made water systems and in moist soil. Over the past 5 years, notification rates of this disease have almost doubled in the European Union (EU) / European Environmental Agency (EEA), from 1.4 in 2015 to 2.2 cases per 100,000 population in 2019. Some studies show that the greater presence of the microorganism in the water network and the increase in cases of legionellosis could be related to the variations in some environmental factors, such as air temperature, which may influence the water temperature.

Study design. Climate change is currently a prominent topic worldwide because of its significant impact on the natural environment. It is responsible for the increase in numerous waterborne pathologies. The purpose of this study was to correlate the air temperature recorded in Apulia region from January 2018 to April 2023 with the presence of Legionella in the water networks of public and private facilities and the incidence rates of legionellosis during the same period.

Methods. During the period from January 2018 to April 2023, water samples were collected from  facilities involved in legionellosis cases and analyzed for Legionella. During the same period, all the cases notified to the regional epidemiological observatory (OER-Apulia) were included in this study. Statistical analyses were conducted using the Shapiro–Wilk test to determine whether the Legionella load was distributed normally, the Wilcoxon rank sum test to compare the air temperatures (average and range) of the negative and positive samples for Legionella detection, and the  multivariate analysis (Poisson regression) to compare the Legionella load with the water sample temperature, average air temperature, and temperature range on the day of sampling. The Wilcoxon test for paired samples was used to compare legionellosis cases between the warmer and colder months.

Results. Overall, 13,044 water samples were analyzed for Legionella and 460 cases of legionellosis were notified. Legionella was isolated in 20.1% of the samples examined. The difference in the air temperature between negative samples and positive samples was statistically significant (p-value < 0.0001): on days when water samples tested positive for Legionella a higher temperature range was observed than on days when water samples tested negative (p-value = 0.004). Poisson regression showed a direct correlation between Legionella load, water temperature, and average air temperature. The incidence of legionellosis cases in warmer months was higher than in colder months (p-value = 0.03).

Conclusions. Our study highlights a significant increase in the load of Legionella in the Apulian water network, and an association between warmer temperatures and legionellosis incidence. In our opinion, further investigations are needed in different contexts and territories to characterize the epidemiology of legionellosis, and to explain its extreme variability in different geographical areas and how these data may be influenced by different risk factors.

References

1. Mora C, McKenzie T, Gaw IM, et al. Over half of known human pathogenic diseases can be aggravated by climate change. Nat Clim Chang.

2022; 12(9): 869-75. doi: 10.1038/s41558-02201426-1. Epub 2022 Aug 8.

2. Dupke S, Buchholz U, Fastner J, et al. Impact of climate change on waterborne infections and intoxications. J Health Monit. 2023 Jun 1; 8(Suppl

3): 62-77. https://doi.org/10.25646/11402.

3. Calero Preciado C, Boxall J, Soria-Carrasco V, Martínez S, Douterelo I. Implications of Climate

Change: How Does Increased Water Temperature Influence Biofilm and Water Quality of Chlorinated Drinking Water Distribution Systems? Front Microbiol. 2021 Jun 8; 12: 658927.

https://doi.org/10.3389/fmicb.2021.658927.

4. World Meteorological Organization (WMO). Statement on the state of the Global Climate; 2020. Available on: public.wmo.int [Last accessed: 2023 June 11].

5. European Food Safety Authority (EFSA) and European Centre for Disease Prevention and Control (ECDC), 2019. The European Union One Health 2018 Zoonoses Report. EFSA J.

2019 Dec 11: e05926. https://doi.org/10.2903/j. efsa.2019.5926.

6. Brandsema PS, Euser SM, Karagiannis I, Den Boer JW, Van Der Hoek W. Summer increase of Legionnaires’ disease 2010 in The Netherlands associated with weather conditions and implications for source finding. Epidemiol Infect. 2014 Nov; 142(11): 2360-71. doi: 10.1017/ S0950268813003476. Epub 2014 Jan 24.

7. Conza L, Casati Pagani S, Gaia V. Influence of climate and geography on the occurrence of Legionella and amoebae in composting facilities. BMC Res Notes. 2014 Nov 24; 7: 831. doi: 10.1186/1756-0500-7-831.

8. Beautè J, Sandini S, Uldum SA, Rota MC, Brandsema P, Giesecke J. Shortterm effects of atmospheric pressure, temperature, and rainfall on notification rate of community-acquired Legionnaires’ disease in four European countries. Epidemiol Infect. 2016 Dec; 144(16): 3483-93. doi: 10.1017/S0950268816001874. Epub 2016 Aug 30.

9. Walker JT. The influence of climate change on waterborne disease and Legionella: a review. Perspect Public Health. 2018 Sep; 138(5): 282-6. doi: 10.1177/1757913918791198.

10. Han XY. Effects of climate changes and road exposure on the rapidly rising legionellosis incidence rates in the United States. PLoS One 2021 Apr 22; 16(4): e0250364. doi: 10.1371/ journal.pone.0250364.

11. Laganà P, Facciolà A, Palermo R, Delia S. Environmental Surveillance of Legionellosis within an Italian University Hospital. Results of 15 Years of Analysis. Int J Environ Res Public Health. 2019; 16(7): 1103. doi:10.3390/ ijerph16071103.

12. De Giglio O, Fasano F, Diella G, et al. Legionella and legionellosis in touristic-recreational facilities: Influence of climate factors and geostatistical analysis in Southern Italy (20012017). Environ Res. 2019 Nov; 178: 108721. doi: 10.1016/j.envres.2019.108721. Epub 2019 Sep 6.

13. Filice S, Sciuto EL, Scalese S, et al. Innovative antibiofilm smart surface against Legionella for water systems. Microorganisms. 2022; 10(5): 870. doi: 10.3390/microorganisms10050870.

14. Sciuto EL, Laganà P, Filice S, et al. Environmental management of Legionella in domestic water systems: consolidated and innovative approaches for disinfection methods and risk assessment. Microorganisms. 2021; 9(3): 577. doi: 10.3390/ microorganisms9030577.

15. Van Heijnsbergen E, de Roda Husman AM, Lodder WJ, et al. Viable Legionella pneumophila bacteria in natural soil and rainwater puddles. J Appl Microbiol. 2014 Sep; 117(3): 882-90. doi: 10.1111/jam.12559. Epub 2014 Jun 26.

16. European Centre for Disease Prevention and Control (ECDC). Legionnaires’ disease. Annual epidemiological report for 2019. Stockholm: ECDC; 2021. Available on: https://www.ecdc. europa.eu/sites/default/files/documents/AERlegionnaires-2019.pdf [Last accessed: 2023 June 19].

17. Ahmed SS, Hunter CM, Mercante JW, et al. Legionnaires’ Disease at a Hotel in Missouri,

2015: The Importance of Environmental Health Expertise in Understanding Water Systems. J Environ Health 2019 Mar; 81(7): 8-13.

18. Barskey AE, Lackraj D, Tripathi PS, Lee S, Smith J, Edens C. Travel-associated cases of

Legionnaires’ disease in the United States, 2015– 2016. Travel Med Infect Dis. 2021 Mar-Apr; 40: 101943. doi: 10.1016/j.tmaid.2020.101943. Epub 2020 Dec 3.

19. List of Prokaryotic Names with Standing in

Nomenclature(LPSN) moves to the DSMZ.

Available on: https://lpsn.dsmz.de/genus/legionella [Last accessed: 2023 July 12].

20. Napoli C, Fasano F, Iatta R, Barbuti G, Cuna T, Montagna MT. Legionella spp. and legionellosis in Southeastern Italy: disease epidemiology and environmental surveillance in community and health care facilities. BMC Public Health. 2010 Nov; 10: 660. doi: 10.1186/1471-2458-10660.

21. Palmer A, Painter J, Hassler H, et al. Legionella clemsonensis sp. nov.: a green fluorescing Legionella strain from a patient with pneumonia. Microbiol Immunol. 2016 Oct; 60(10): 694-701. doi: 10.1111/1348-0421.12439.

22. Relich RF, Schmitt BH, Raposo H, Barker L, Blosser SJ, May M. Legionella indianapolisensis sp. nov., isolated from a patient with pulmonary abscess. Int J Infect Dis. 2018 Apr; 69: 26-8. doi: 10.1016/j.ijid.2018.01.024. Epub 2018 Feb 1.

23. De Giglio O, D’Ambrosio M, Spagnuolo V, et al. Legionella anisa or Legionella bozemanii? Traditional and molecular techniques as support in the environmental surveillance of a hospital water network. Environ Monit Assess. 2023 Mar 22; 195(4): 496. doi: 10.1007/s10661-023 -11078-z.

24. Edelstein PH, Roy CR. Legionnaires’ disease and Pontiac fever. In: Bennett JE, Dolin R, Blaser MJ, Eds. Mandell, Douglas, and Bennett’s Principles and Practice of Infectious Diseases. 8th ed. Philadelphia: PA. Saunders, 2015: 293344.

25. Napoli C, De Giglio O, Bertamino E, Montagna MT. Legionellosis in health care facilities: state of the art in control and prevention in Italy. Ann Ig. 2019 Sep-Oct; 31(5): 474-81. doi: 10.7416/ ai.2019.2308.

26. Paniagua AT, Paranjape K, Hu M, Bédard E, Faucher SP. Impact of temperature on Legionella pneumophila, its protozoan host cells, and the microbial diversity of the biofilm community of a pilot cooling tower. Sci Total Environ. 2020 Apr; 712: 136131. doi: 10.1016/j.

scitotenv.2019.136131. Epub 2019 Dec 28.

27. Carvalho FRS, Nastasi FR, Gamba RC, Foronda AS, Pellizari VH. Occurrence and diversity of Legionellaceae in polar Lakes of the Antarctic Peninsula. Curr Microbiol. 2008 Oct; 57(4): 294-300. doi: 10.1007/s00284-008-9192-y. Epub 2008 Jun 28.

28. Graells T, Ishak H, Larsson M, Guy L. The allintracellular order Legionellales is unexpectedly diverse, globally distributed and lowly abundant. FEMS Microbiol Ecol 2018 Dec 1; 94(12): fiy185. doi: 10.1093/femsec/fiy185.

29. Portale dell’Osservatorio Epidemiologico regionale. Available on: https://www.sanita.puglia. it/osservatorio-epidemiologico-regionale [Last accessed 2023 May 16].

30. Montagna MT, Napoli C, Tatò D, Spilotros G, Barbuti G, Barbuti S. Clinical environmental surveillance of legionellosis: an experience in Southern Italy. Eur J Epidemiol. 2006; 21(4): 325-31. doi: 10.1007/s10654-006-0009-7.

31. Montagna MT, Cuna T, De Giglio O, Bollino A, Iatta R, Napoli C. Spa facilities and legionellosis: legislative structure and state of the art in Apulia (Italy). Ig Sanita Pubbl. 2012 Sep-Oct; 68(5): 719-31.

32. Montagna MT, De Giglio O, Cristina ML, et al. Evaluation of Legionella air contamination in healthcare facilities by different sampling methods: an Italian multicenter study. Int J Environ Res Public Health. 2017 Jun 22; 14(7): 670. doi:

10.3390/ijerph14070670.

33. Napoli C, Iatta R, Fasano F, Marsico T, Montagna MT. Variable bacterial load of Legionella spp. in a hospital water system. Sci Total Environ. 2009 Dec 20; 408(2): 242-4. doi: 10.1016/j. scitotenv.2009.09.039.

34. Napoli C, Iatta R, Fasano F, Marsico T, Montagna MT. [Legionella and Legionellosis in Apulia. (Southern-Italy): epidemiology and surveillance in the years 2000-2008]. Ann Ig. 2009; 21(Suppl 1): 181-8.

35. ISO 11731:2017. Water quality-enumeration of Legionella. Available on: https://www.iso.org/ standard/61782.html [Last accessed: 2023 May 16].

36. Portale della Protezione Civile Puglia. Available on: https://protezionecivile.puglia.it/bollettinimeteorologici-regionali-mensili [Last accessed: 2023 May 16].

37. Wookey P, Aerts R, Bardgett RD, et al. Ecosystem feedbacks and cascade processes: understanding their role in the responses of Arctic and alpine ecosystems to environmental change. Glob Change Biol. 2009; 15(5): 1153-72. https:// doi.org/10.1111/j.1365-2486.2008.01801.x.

38. Andrade L, O’Dwyer J, O’Neill E, Hynds P. Surface water flooding, groundwater contamination, and enteric disease in developed countries: a scoping review of connections and consequences. Environ Pollut. 2018 May; 236: 540-9. doi: 10.1016/j.envpol.2018.01.104.

39. Levy K, Smith SM, Carlton EJ. Climate change impacts on waterborne diseases: moving toward designing interventions. Curr Environ Health Rep. 2018 Jun; 5(2): 272-82. doi: 10.1007/ s40572-018-0199-7.

40. Dupke S, Buchholz U, Fastner J, et al. Impact of climate change on waterborne infections and intoxications. J Health Monit. 2023 Jun 1; 8(Suppl 3): 62-77. doi: 10.25646/11402.

41. O’Keeffe J. Climate change and opportunistic pathogens (OPs) in the built environment. Environ Health Rev. 2022 Oct 13; 65(3): 69-76.

https://doi.org/10.5864/d2022-016.

42. Quero S, Párraga-Niño N, Garcia-Núñez M, et al. The impact of pipeline changes and temperature increase in a hospital historically colonised with Legionella. Sci Rep. 2021 Jan 21; 11(1): 1916.

doi: 10.1038/s41598-021-81625-6.

43. Health Technical Memorandum (HTM) 04-01: Safe water in healthcare premises. Available on: https://www.england.nhs.uk/publication/ safe-water-in-healthcare-premises-htm-04-01/, 2016 [Last accessed: 2023 June 24].

44. Fisman DN, Lim S, Wellenius GA, 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. doi: 10.1086/498248. Epub 2005 Nov 11.

45. Vermeulen LC, Brandsema PS, van de Kassteele J, et al. Atmospheric dispersion and transmission of Legionella from wastewater treatment plants: A 6-year case-control study. Int J Hyg Environ Health. 2021 Aug; 237: 113811. doi: 10.1016/j. ijheh.2021.113811. Epub 2021 Jul 23.

46. Wallet F, Fontenay L, Cabanes PA. Probabilistic analysis of a French legionellosis outbreak shows potential role of wastewater basin. Microorganisms. 2022 Feb 11; 10(2): 422. doi:

10.3390/microorganisms10020422.

47. De Giglio O, Napoli C, Apollonio F. et al. Occurrence of Legionella in groundwater used for sprinkler irrigation in Southern Italy. Environ Res. 2019 Mar; 170: 215-21. doi: 10.1016/j.

envres.2018.12.041. Epub 2018 Dec 19.

48. Passer JK, Danila RN, Laine ES, Como-Sabetti KJ, Tang W, Searle KM. The association between sporadic Legionnaires’ disease and weather and environmental factors, Minnesota, 2011–2018. Epidemiol Infect. 2020 Jun 29; 148: e156. doi: 10.1017/S0950268820001417.

49. Rhoads WJ, Sindelar M, Margot C, Graf N, Hammes F. Variable Legionella Response to Building Occupancy Patterns and Precautionary Flushing. Microorganisms. 2022 Mar 3; 10(3): 555. doi: 10.3390/microorganisms10030555.

50. De Giglio O, Diella G, Lopuzzo M, et al. Impact of lockdown on the microbiological status of the hospital water network during COVID-19 pandemic. Environ Res. 2020 Sep 22: 110231. doi: 10.1016/j.envres.2020.110231.

Downloads

Published

2025-08-04

Issue

Section

Original research

How to Cite

1.
Montagna MT, Brigida S, Fasano F, et al. The role of air temperature in Legionella water contamination and legionellosis incidence rates in southern Italy (2018–2023). Ann Ig. 2025;35(6):631-640. doi:10.7416/ai.2023.2578