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      Effects of climate changes and road exposure on the rapidly rising legionellosis incidence rates in the United States

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          Abstract

          Legionellosis is an infection acquired through inhalation of aerosols that are contaminated with environmental bacteria Legionella spp. The bacteria require warm temperature for proliferation in bodies of water and moist soil. The legionellosis incidence in the United States has been rising rapidly in the past two decades without a clear explanation. In the meantime, the US has recorded consecutive years of above-norm temperature since 1997 and precipitation surplus since 2008. The present study analyzed the legionellosis incidence in the US during the 20-year period of 1999 to 2018 and correlated with concurrent temperature, precipitation, solar ultraviolet B (UVB) radiation, and vehicle mileage data. The age-adjusted legionellosis incidence rates rose exponentially from 0.40/100,000 in 1999 (with 1108 cases) to 2.69/100,000 in 2018 (with 9933 cases) at a calculated annual increase of 110%. In regression analyses, the rise correlated with an increase in vehicle miles driven and with temperature and precipitation levels that have been above the 1901–2000 mean since 1997 and 2008, respectively, suggesting more road exposure to traffic-generated aerosols and promotive effects of anomalous climate. Remarkably, the regressions with cumulative anomalies of temperature and precipitation were robust (R 2 ≥ 0.9145, P ≤ 4.7E-11), implying possible changes to microbial ecology in the terrestrial and aquatic environments. An interactive synergy between annual precipitation and vehicle miles was also found in multiple regressions. Meanwhile, the bactericidal UVB radiation has been decreasing, which also contributed to the rising incidence in an inverse correlation. The 2018 legionellosis incidence peak corresponded to cumulative effects of the climate anomalies, vast vehicle miles (3,240 billion miles, 15904 km per capita), record high precipitation (880.1 mm), near record low UVB radiation (7488 kJ/m 2), and continued above-norm temperature (11.96°C). These effects were examined and demonstrated in California, Florida, New Jersey, Ohio, and Wisconsin, states that represent diverse incidence rates and climates. The incidence and above-norm temperature both rose most in cold Wisconsin. These results suggest that warming temperature and precipitation surplus have likely elevated the density of Legionella bacteria in the environment, and together with road exposure explain the rapidly rising incidence of legionellosis in the United States. These trends are expected to continue, warranting further research and efforts to prevent infection.

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          Most cited references42

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          Legionella and Legionnaires' disease: 25 years of investigation.

          There is still a low level of clinical awareness regarding Legionnaires' disease 25 years after it was first detected. The causative agents, legionellae, are freshwater bacteria with a fascinating ecology. These bacteria are intracellular pathogens of freshwater protozoa and utilize a similar mechanism to infect human phagocytic cells. There have been major advances in delineating the pathogenesis of legionellae through the identification of genes which allow the organism to bypass the endocytic pathways of both protozoan and human cells. Other bacteria that may share this novel infectious process are Coxiella burnetti and Brucella spp. More than 40 species and numerous serogroups of legionellae have been identified. Most diagnostic tests are directed at the species that causes most of the reported human cases of legionellosis, L. pneumophila serogroup 1. For this reason, information on the incidence of human respiratory disease attributable to other species and serogroups of legionellae is lacking. Improvements in diagnostic tests such as the urine antigen assay have inadvertently caused a decrease in the use of culture to detect infection, resulting in incomplete surveillance for legionellosis. Large, focal outbreaks of Legionnaires' disease continue to occur worldwide, and there is a critical need for surveillance for travel-related legionellosis in the United States. There is optimism that newly developed guidelines and water treatment practices can greatly reduce the incidence of this preventable illness.
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            Distribution of Legionella species and serogroups isolated by culture in patients with sporadic community-acquired legionellosis: an international collaborative survey.

            This international collaborative survey identified culture-confirmed legionellosis in 508 patients with sporadic community-acquired legionellosis. Legionella pneumophila constituted 91.5% of the isolates. Serogroup 1 was the predominant serogroup (84.2%), and serogroups 2-13 (7.4%) accounted for the remaining serogroups. The Legionella species most commonly isolated were L. longbeachae (3.9%) and L. bozemanii (2.4%), followed by L. micdadei, L. dumoffii, L. feeleii, L. wadsworthii, and L. anisa (2.2% combined). L. longbeachae constituted 30.4% of the community-acquired Legionella isolates in Australia and New Zealand.
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              Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory disease.

              To identify the etiologic agent of Legionnaire's disease, we examined patients' serum and tissue specimens in a search for toxins, bacteria, fungi, chlamydiae, rickettsiae and viruses. From the lungs of four of six patients we isolated a gram-negative, non-acid-fast bacillus in guinea pigs. The bacillus could be transferred to yolk sacs of embryonated eggs. Classification of this organism is incomplete. We used yolk-sac cultures of the bacillus as antigen to survey suspected serum specimens, employing antihuman-globulin fluorescent antibody. When compared to controls, specimens from 101 to 111 patients meeting clinical criteria of Legionnaires' disease showed diagnostic increases in antibody titers. Diagnostic increases were also found in 54 recent sporadic cases of severe pneumonia and, retrospectively, in stored serum from most patients in two other previously unsolved outbreaks of respiratory disease. We conclude that Legionnaires' disease is caused by a gram-negative bacterium that may be responsible for widespread infection.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                22 April 2021
                2021
                : 16
                : 4
                : e0250364
                Affiliations
                [001]Department of Laboratory Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX, United States of America
                Universite du Quebec a Montreal, CANADA
                Author notes

                Competing Interests: The author has declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-8472-0870
                Article
                PONE-D-20-33121
                10.1371/journal.pone.0250364
                8061983
                33886659
                92e1427a-398a-4173-9c88-2a0504b21b90
                © 2021 Xiang Y. Han

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 21 October 2020
                : 30 March 2021
                Page count
                Figures: 5, Tables: 3, Pages: 19
                Funding
                The author received no specific funding for the work.
                Categories
                Research Article
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Bacterial Diseases
                Legionellosis
                Medicine and Health Sciences
                Epidemiology
                Physical sciences
                Physics
                Electromagnetic radiation
                Light
                Ultraviolet radiation
                Ultraviolet B
                Engineering and Technology
                Civil Engineering
                Transportation Infrastructure
                Roads
                Engineering and Technology
                Transportation
                Transportation Infrastructure
                Roads
                Physical Sciences
                Materials Science
                Materials
                Mixtures
                Aerosols
                Physical Sciences
                Physics
                Electromagnetic Radiation
                Solar Radiation
                Earth Sciences
                Atmospheric Science
                Meteorology
                Rain
                People and places
                Geographical locations
                North America
                United States
                Custom metadata
                All relevant data are within the paper.

                Uncategorized
                Uncategorized

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