Vital Signs: Deficiencies in Environmental Control Identified in Outbreaks of Legionnaires’ Disease—North America, 2000–2014

Abstract

Background: The number of reported cases of Legionnaires’ disease, a severe pneumonia caused by the bacterium Legionella, is increasing in the United States. During 2000–2014, the rate of reported legionellosis cases increased from 0.42 to 1.62 per 100 000 persons; 4% of reported cases were outbreak-associated. Legionella is transmitted through aerosolization of contaminated water. A new industry standard for prevention of Legionella growth and transmission in water systems in buildings was published in 2015. CDC investigated outbreaks of Legionnaires’ disease to identify gaps in building water system maintenance and guide prevention efforts.Methods: Information from summaries of CDC Legionnaires’ disease outbreak investigations during 2000–2014 was systematically abstracted, and water system maintenance deficiencies from land-based investigations were categorized as process failures, human errors, equipment failures, or unmanaged external changes.Results: During 2000–2014, CDC participated in 38 field investigations of Legionnaires’ disease. Among 27 land-based outbreaks, the median number of cases was 10 (range = 3–82) and median outbreak case fatality rate was 7% (range = 0–80%). Sufficient information to evaluate maintenance deficiencies was available for 23 (85%) investigations. Of these, all had at least one deficiency; 11 (48%) had deficiencies in ≥2 categories. Fifteen cases (65%) were linked to process failures, 12 (52%) to human errors, eight (35%) to equipment failures, and eight (35%) to unmanaged external changes.Conclusions and Implications for Public Health Practice: Multiple common preventable maintenance deficiencies were identified in association with disease outbreaks, highlighting the importance of comprehensive water management programs for water systems in buildings. Properly implemented programs, as described in the new industry standard, could reduce Legionella growth and transmission, preventing Legionnaires’ disease outbreaks and reducing disease. Background: The number of reported cases of Legionnaires’ disease, a severe pneumonia caused by the bacterium Legionella, is increasing in the United States. During 2000–2014, the rate of reported legionellosis cases increased from 0.42 to 1.62 per 100 000 persons; 4% of reported cases were outbreak-associated. Legionella is transmitted through aerosolization of contaminated water. A new industry standard for prevention of Legionella growth and transmission in water systems in buildings was published in 2015. CDC investigated outbreaks of Legionnaires’ disease to identify gaps in building water system maintenance and guide prevention efforts. Methods: Information from summaries of CDC Legionnaires’ disease outbreak investigations during 2000–2014 was systematically abstracted, and water system maintenance deficiencies from land-based investigations were categorized as process failures, human errors, equipment failures, or unmanaged external changes. Results: During 2000–2014, CDC participated in 38 field investigations of Legionnaires’ disease. Among 27 land-based outbreaks, the median number of cases was 10 (range = 3–82) and median outbreak case fatality rate was 7% (range = 0–80%). Sufficient information to evaluate maintenance deficiencies was available for 23 (85%) investigations. Of these, all had at least one deficiency; 11 (48%) had deficiencies in ≥2 categories. Fifteen cases (65%) were linked to process failures, 12 (52%) to human errors, eight (35%) to equipment failures, and eight (35%) to unmanaged external changes. Conclusions and Implications for Public Health Practice: Multiple common preventable maintenance deficiencies were identified in association with disease outbreaks, highlighting the importance of comprehensive water management programs for water systems in buildings. Properly implemented programs, as described in the new industry standard, could reduce Legionella growth and transmission, preventing Legionnaires’ disease outbreaks and reducing disease. Legionnaires’ disease, a severe, sometimes fatal pneumonia, can occur in persons who inhale aerosolized droplets of water contaminated with the bacterium Legionella. Exposure to Legionella in freshwater environments such as lakes and streams does not lead to disease; however, in manmade water systems, Legionella can grow and spread to susceptible hosts, including persons aged ≥50 years, smokers, and persons with underlying medical conditions such as chronic lung disease or immunosuppression. CDC investigated the first outbreak of Legionnaires’ disease in 1976. Currently, approximately 5000 cases of Legionnaires’ disease are reported to CDC each year; however, Legionnaires’ disease might be underdiagnosed. During 2000–2014, the rate of reported cases of legionellosis, which comprises both Legionnaires’ disease and Pontiac fever, a milder, self-limited, influenza-like illness, increased 286%, from 0.42 to 1.62 cases per 100 000 persons in the United States (1Adams D Fullerton K Jajosky R et al.Summary of notifiable infectious diseases and conditions—United States, 2013.MMWR Morb Mortal Wkly Rep. 2015; 62: 1-122Crossref PubMed Scopus (94) Google Scholar, 2CDC. Notice to readers: Final 2014 reports of nationally notifiable infectious diseases.MMWR Morb Mortal Wkly Rep. 2015; 64: 1019-1033Crossref Scopus (17) Google Scholar) (Figure 1). The reason for this increase is unknown but is likely multifactorial. The higher rates could represent a true increase in the frequency of disease related to several factors, such as a greater number of persons at risk for legionellosis because of underlying illness or immunocompromising medications, an aging U.S. population, aging plumbing infrastructure, or changes in the climate. Increased use of diagnostic testing because of greater awareness among clinicians and availability of diagnostic tests, as well as more reliable reporting to local and state health departments and CDC could also be playing a role. Approximately 9% of cases are fatal (3Dooling KL Toews KA Hicks LA et al.Active bacterial core surveillance for legionellosis—United States, 2011–2013.MMWR Morb Mortal Wkly Rep. 2015; 64: 1190-1193Crossref PubMed Scopus (76) Google Scholar). Among 32 potable water–associated outbreaks reported in the United States during 2011–2012, legionellosis was implicated in 21 (66%) outbreaks and all 14 deaths (4Beer KD Gargano JW Roberts VA et al.Surveillance for waterborne disease outbreaks associated with drinking water—United States, 2011–2012.MMWR Morb Mortal Wkly Rep. 2015; 64: 842-848Crossref PubMed Scopus (160) Google Scholar). During 2000–2012, CDC's Waterborne Disease and Outbreak Surveillance System received reports of approximately 160 legionellosis outbreaks (5CDC. Waterborne disease and outbreak surveillance system. Atlanta, GA: US Department of Health and Human Services, CDC; 2016. Available from: http://www.cdc.gov/healthywater/surveillance/surveillance-reports.html.Google Scholar). Legionnaires’ disease outbreak investigations require an environmental assessment to identify potential sources of exposure. Environmental assessments are rarely conducted for Legionnaires’ disease cases that are not recognized as part of an outbreak; therefore, most of what is known about Legionella transmission has been learned from outbreak investigations. During 2005–2009, only 4% of confirmed legionellosis cases reported among U.S. residents were associated with a known outbreak or cluster (6Hicks LA Garrison LE Nelson GE et al.Legionellosis—United States, 2000–2009.MMWR Morb Mortal Wkly Rep. 2011; 60: 1083-1086PubMed Google Scholar), although some sporadic cases were likely associated with unrecognized outbreaks or clusters. Identified outbreaks generally are linked to environmental reservoirs in large or complex water systems, *Large or complex water systems, where Legionella can grow and spread, are most often associated with commercial, institutional, multiunit residential, health care, and industrial buildings, often with multiple stories and complicated plumbing systems. Buildings in which vulnerable populations, such as immunocompromised or elderly persons, live or are treated are also considered to have complex water systems. such as those found in hotels or resorts, hospitals, long-term care facilities, and cruise ships. Transmission from these water systems to humans requires aerosol generation, as can occur from showerheads, cooling towers, hot tubs, and decorative fountains (7Fields BS Benson RF Besser RE Legionella and Legionnaires’ disease: 25 years of investigation.Clin Microbiol Rev. 2002; 15: 506-526Crossref PubMed Scopus (1276) Google Scholar). Only one case of possible person-to-person transmission has been reported (8Correia AM Ferreira JS Borges V et al.Probable person-to-person transmission of Legionnaires’ disease.N Engl J Med. 2016; 374: 497-498Crossref PubMed Scopus (135) Google Scholar). Legionnaires’ disease is typically diagnosed by a Legionella urinary antigen test or culture of lower respiratory secretions using selective media; epidemiologic links to environmental sources can be confirmed when isolates from clinical and environmental specimens match by molecular typing (9Mercante JW Winchell JM Current and emerging Legionella diagnostics for laboratory and outbreak investigations.Clin Microbiol Rev. 2015; 28: 95-133Crossref PubMed Scopus (211) Google Scholar). One species, Legionella pneumophila, accounts for approximately 90% of reported legionellosis cases in the United States (7Fields BS Benson RF Besser RE Legionella and Legionnaires’ disease: 25 years of investigation.Clin Microbiol Rev. 2002; 15: 506-526Crossref PubMed Scopus (1276) Google Scholar). Because Legionella transmission occurs from manmade environmental settings, the most effective strategy for prevention of Legionnaires’ disease is through control of Legionella in water systems in buildings. In 2015, ASHRAE (formerly known as the American Society of Heating, Refrigerating, and Air-Conditioning Engineers) published a consensus standard for the primary prevention of Legionnaires’ disease (10ASHRAE. Legionellosis: Risk management for building water systems. ANSI/ASHRAE Standard 188–2015. Atlanta, GA: ASHRAE; 2015. Available from: http://www.mesc.org/downloads/v/PCTI/ASHRAE%20188%20-%202015%20FINAL.pdf.Google Scholar), which calls for the development and implementation of water management programs in large or complex water systems in buildings. The standard, which is based on best practices, focuses on identifying hazardous conditions and applying control measures to interrupt Legionella growth and transmission. Outbreak investigations often find manmade water systems with maintenance gaps that permit the growth of Legionella. To identify opportunities for prevention, summaries of all CDC field investigations of outbreaks of Legionnaires’ disease during 2000–2014 were reviewed to characterize water system maintenance deficiencies leading to those outbreaks. CDC offers assistance to health departments with field investigations of outbreaks of Legionnaires’ disease. After each investigation, CDC reviews and summarizes the field notes to understand conditions that led to the outbreak. These summaries highlight the main findings from each investigation, including the numbers of cases and deaths, clinical or environmental strains of Legionella identified, potential or confirmed environmental sources, and possible environmental factors that contributed to the outbreak, as well as recommended solutions for the management of current outbreaks and prevention of future outbreaks. CDC reviewed all investigation summaries and associated publications describing Legionnaires’ disease outbreak investigations conducted during 2000–2014. Investigations involving cruise ships were excluded, because their water systems are managed differently from land-based water systems. Two investigators used a standard abstraction form to review the relevant materials. Confirmed and suspected Legionnaires’ disease cases were defined using each outbreak's case definitions; thus, slight variations in case definition among outbreaks were possible. Investigation summaries were reviewed to identify possible root causes that could facilitate Legionella growth and transmission. Each reviewer independently assigned findings to one or more of four categories: (1) process failures, in which a process, such as a water management program, was missing or inadequate; (2) human errors, in which a person did not perform as expected, such as not replacing hot tub filters according to manufacturer's recommendations; (3) equipment failures, in which a piece of equipment did not operate as expected, such as a malfunctioning disinfectant delivery system; and (4) unmanaged external changes, in which adjustments were not made to account for events outside a building water system, such as nearby construction leading to changes in potable water quality. Discrepant categorizations were resolved through consultation with a third reviewer. During 2000–2014, CDC participated in 38 field investigations of Legionnaires’ disease. Three investigations, determined not to be outbreaks because of lack of sufficient clinical or epidemiologic evidence, were excluded. Eight investigations involving cruise ships, associated with 19 confirmed and 17 suspected cases of Legionnaires’ disease, including two deaths, were also excluded. Among the remaining 27 investigations, 24 occurred in U.S. states and territories, two in Mexico, and one in Canada. The most frequent outbreak settings were hotels and resorts (n = 12, 44%), long-term care facilities (5, 19%), and hospitals (4, 15%) (Table 1). The remaining six outbreaks were evenly distributed among senior living facilities (n = 2, 7%), workplaces (2, 7%), and the community (2, 7%). Potable water was the most frequent source of exposure (n = 15, 56%), followed by cooling towers (6, 22%), hot tubs (2, 7%), industrial equipment (1, 4%), and a decorative fountain (1, 4%); for two outbreaks (7%), sources were not identified (Figure 2). Potable water sources accounted for 58% of travel-associated outbreaks (in hotels and resorts) and 67% of health care–associated outbreaks (in hospitals and long-term care facilities).Table 1CDC field investigations of Legionnaires’ disease outbreaks–North America, 2000–20141Excludes one pseudo-outbreak, two non-outbreaks, and eight cruise ship outbreaks. (n = 27)Year of investigationSettingSourceEnvironmental and clinical isolate match2On the basis of DNA-sequence–based typing.No. confirmed and suspected casesNo. deathsCase fatality rate (%)Total3For the purposes of this analysis, cases of confirmed and suspect Legionnaires’ disease were defined using each outbreak's case definition.Confirmed3For the purposes of this analysis, cases of confirmed and suspect Legionnaires’ disease were defined using each outbreak's case definition.Suspected3For the purposes of this analysis, cases of confirmed and suspect Legionnaires’ disease were defined using each outbreak's case definition.2001WorkplaceIndustrial equipmentNo4402502001Hotel/ResortPotable waterYes21516152002Long-term care facilityPotable waterYes311219262003Hotel/ResortPotable waterNo clinical isolate330002004Hotel/ResortPotable waterNo clinical isolate871002004Hotel/ResortHot tubNo environmental or clinical isolate651002004CommunityCooling towerNo clinical isolate9722222005CommunityDecorative fountainYes18180162005Long-term care facilityCooling towerYes8282023282006HospitalPotable waterYes101003302006Senior living facilityPotable waterNo clinical isolate633002008Hotel/ResortPotable waterYes13112002009Senior living facilityPotable waterYes101001102010Hotel/ResortPotable waterYes11101002010Hotel/ResortCooling towerYes8621132010WorkplaceCooling towerYes29722002011HospitalPotable waterNo clinical isolate13310182011Hotel/ResortUnknown4Decorative fountain suspected; potable water/hot tub not excluded.No environmental or clinical isolate330002011Long-term care facilityPotable waterNo clinical isolate10468802011Hotel/ResortPotable waterNo clinical isolate550002012HospitalPotable water (possibly also decorative fountain)Yes212105242013Long-term care facilityUnknownNo191545262013Hotel/ResortCooling towerNo clinical isolate15150172013Long-term care facilityCooling towerYes413926152013Hotel/ResortHot tubNo environmental isolate431002014Hotel/ResortPotable water (and possibly hot tub)No clinical isolate6601172014HospitalPotable waterYes990222Total415323926575Median.1 Excludes one pseudo-outbreak, two non-outbreaks, and eight cruise ship outbreaks.2 On the basis of DNA-sequence–based typing.3 For the purposes of this analysis, cases of confirmed and suspect Legionnaires’ disease were defined using each outbreak's case definition.4 Decorative fountain suspected; potable water/hot tub not excluded.3 Median. Open table in a new tab All 27 outbreaks were caused by Legionella pneumophila serogroup 1. Among 13 (48%) investigations (Table 1), links between human cases and water sources were established through DNA-sequence–based typing that identified indistinguishable clinical and environmental isolates. No clinical isolate was available for nine (33%) outbreaks, no environmental isolate was available for one (4%), and neither a clinical nor environmental isolate was available for two (7%); the clinical and environmental isolates did not match for the remaining two (7%) outbreaks. All available outbreak strains reacted with monoclonal antibody 2 of the international L. pneumophila serogroup 1 panel, a potential marker of increased virulence (11Kozak NA Benson RF Brown E et al.Distribution of lag-1 alleles and sequence-based types among Legionella pneumophila serogroup 1 clinical and environmental isolates in the United States.J Clin Microbiol. 2009; 47: 2525-2535Crossref PubMed Scopus (66) Google Scholar). The 27 outbreaks included 415 cases, 323 (78%) of which were confirmed †For comparison, an estimated 41 500 cases of confirmed cases of Legionnaires’ disease were reported to CDC during 2000–2014 (unpublished data). and 92 (22%) suspected (Table 1). A median of 10 confirmed and suspected cases occurred in each outbreak (range = 3–82). The median number of cases in cooling tower outbreaks was 22, and in potable water outbreaks was 10. Health care–associated outbreaks accounted for 57% of all 415 cases, with a median of 19 cases per health care–associated outbreak; travel-associated outbreaks accounted for 25% of cases, with a median of seven cases per travel-associated outbreak. Among confirmed and suspected Legionnaires’ disease cases, 65 deaths occurred; the median outbreak case fatality rate was 7% (range = 0–80%). Health care–associated outbreaks accounted for 85% of deaths (median health care–associated outbreak case fatality rate = 24%, range = 6–80%); travel-associated outbreaks accounted for 6% of deaths (median travel-associated outbreak case fatality rate = 0%, range = 0–17%). Patients in seven of the nine health care–associated outbreaks included persons who were employees, visitors, or outpatients who did not stay overnight at the facility. No transplant patients were among the health care–associated cases. In 23 investigations for which the outbreak duration could be determined, the median interval from onset of the first to last cases was 49 days. Median outbreak duration was longer for potable water outbreaks (98 days) than for outbreaks linked to other sources (28 days). Twenty-three (85%) investigation summaries had sufficient information to evaluate the contribution of deficiencies in water system maintenance to the outbreak (Table 2). The most frequent deficiencies noted were categorized as process failures (n = 15, 65%), followed by human errors (12, 52%), equipment failures (8, 35%), and unmanaged external changes (8, 35%). For 11 (48%) outbreaks, deficiencies in more than one category were reported. Sixteen (70%) investigations reported inadequate water disinfectant levels and 12 (52%) reported water temperatures in the optimal range for Legionella growth (12ASHRAE. Minimizing the risk of legionellosis associated with building water systems. ASHRAE guideline 12-2000. Atlanta, GA: ASHRAE; 2000. Available from: http://legionella.org/publications/non-visible/ashrae-guideline-12-2000/.Google Scholar). §Although Legionella has been recovered from water with temperatures outside this range, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at temperatures <20°C (<68°F), whereas hot water should be stored at >60°C (>140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at ≥49°C (≥120°F). Indications of inadequate maintenance of hot tubs and decorative fountains were almost always noted. Among the seven investigations where outbreaks were believed to be associated with unmanaged external changes, nearby construction (n = 3, 43%) and problems with water mains (3, 43%) were most frequently noted. Three buildings had water management programs (all developed before the publication of ASHRAE's standard in 2015); however, the occurrence of outbreaks suggests that the existing water management programs were inadequate (13Demirjian A Lucas CE Garrison LE et al.The importance of clinical surveillance in detecting Legionnaires’ disease outbreaks: A large outbreak in a hospital with a Legionella disinfection system—Pennsylvania, 2011–2012.Clin Infect Dis. 2015; 60: 1596-1602Crossref PubMed Scopus (56) Google Scholar,14Silk BJ Moore MR Bergtholdt M et al.Eight years of Legionnaires’ disease transmission in travellers to a condominium complex in Las Vegas, Nevada.Epidemiol Infect. 2012; 140: 1993-2002Crossref PubMed Scopus (20) Google Scholar).Table 2Deficiencies in water system maintenance contributing to growth and transmission of Legionella among outbreaks of Legionnaires’ disease investigated by CDC—North America, 2000–2014 (n = 23)SettingSourceDeficiencyCategory1Each reviewer independently assigned findings to one or more of four categories: (1) process failures, in which a process, such as a water management program, was missing or is inadequate; (2) human errors, in which a person did not perform as expected (e.g. not replacing hot tub filters according to manufacturer's recommendations); (3) equipment failures, in which a piece of equipment did not operate as expected (e.g. a malfunctioning disinfectant delivery system); and (4) unmanaged external changes, in which adjustments were not made to account for events outside a building water system (e.g. nearby construction leading to changes in potable water quality).Process failureHuman errorEquipment failureUnmanaged external changeHotel/ResortPotable waterTemperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in cold potable water✔Hotel/ResortPotable waterTemperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in potable water✔Hotel/ResortPotable waterTemperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in potable waterInadequate disinfectant in potable water✔Hotel/ResortPotable waterTemperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in hot water heaters and in potable waterInadequate disinfectant in potable water, including water coming from supplierStagnation3Water stagnation encourages biofilm growth, reduces temperature, and reduces levels of disinfectant. because of large amounts of water storage and closed wing with unused potable water system (because of low occupancy)✔Hotel/ResortPotable waterTemperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in both hot and cold potable waterInadequate disinfectant in potable waterWater temperature in hot water heater lower than indicated on thermostat✔✔Hotel/ResortPotable waterTemperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in potable waterLegionella water management program (in place as a result of previous outbreak) not comprehensive (i.e. disinfectant not monitored, and remediation performed on a room-by-room basis at certain action thresholds only)Inadequate disinfectant in potable water because of installation of chlorine dioxide injector before the hot water heaters, and occasional mechanical failures of the disinfectant pumps✔✔✔Hotel/ResortPotable water (and possibly also hot tub)Temperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in potable waterLack of disinfectant in potable water (resort served by well water, disinfectant not required by state law)Lack of potable water distribution mapping plans (staff unable to describe system)Poor access to filters and disinfectant feeder because of hot tub placement and equipment designBroken water main4Broken water mains lead to changes in water pressure which can dislodge biofilm (thereby freeing Legionella into water entering the building) and can introduce particulate matter into water entering the building (which can consume disinfectant). (not followed by appropriate flushing of the distribution system)✔✔✔✔Hotel/ResortHot tubInadequate maintenance of hot tubLack of knowledge by contracted pool operator✔Hotel/ResortHot tubInadequate disinfectant in hot tub water because of inaccurate disinfectant feeding equipment, resulting in inadequate disinfectant delivery (unrecognized by hot tub operator)Inadequate hot tub maintenance and disinfectant monitoringUnenforced limits on bather loadsImproper air circulation because of dysfunctional exhaust vents of dehumidifier in pool room, leading to increased exposure to aerosolized bacteria✔✔Hotel/ResortCooling towerInadequate disinfectant in cooling tower because of irregular addition of disinfectant by contractorInadequate record keeping✔Hotel/ResortUnknown (suspected to be a decorative fountain, but possibly potable water or hot tub)Temperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in potable waterInadequate disinfectant in potable water and hot tubsDisinfectant not routinely added to decorative fountain, inadequate maintenance of decorative fountain suspected (but fountain was hyperchlorinated before testing)✔✔HospitalPotable waterHospital under major construction5Vibrations and changes in water pressure experienced during construction can dislodge biofilm and free Legionella into the water entering the building. at time of outbreak (Legionella found in potable water almost exclusively in new building)✔HospitalPotable waterTemperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). at hot water storage tankInadequate disinfectant in potable waterUse of tap water in personal respiratory deviceInsufficient clinical testing for Legionella among patients with pneumonia meeting criteria for possible Legionnaires’ disease✔✔HospitalPotable waterExisting Legionella risk-reduction plan inadequate (Legionella consistently found in hospital potable water)Inadequate disinfectant in potable water (documented by hospital and not addressed)Insufficient clinical testing for Legionella among patients with health care–associated pneumonia✔✔✔Failure of hospital to implement water restrictions upon detecting contamination with Legionella in potable water and associated cases of Legionnaires’ diseaseFailure of hospital to notify public health officials of a recognized outbreak of Legionnaires’ diseaseStagnation3Water stagnation encourages biofilm growth, reduces temperature, and reduces levels of disinfectant. following plumbing inspection and flushing 2 months before occupation of new hematology-oncology unitHospitalPotable water (and possibly also decorative fountain)Inadequate chlorine in potable waterLegionella water management program not comprehensive (i.e. testing for disinfectant and pH in potable water not required)Failure to recognize cases of Legionnaires’ disease as being health care-associatedDelayed reaction to contamination of potable water with Legionella because of(1) Unrecognized contamination (decreased sensitivity of samples because of small volume)(2) Reliance upon action threshold to prompt remediation (when health care–associated cases occurred below threshold)Failure of copper-silver ionization system to control Legionella colonization in hospitalExtensive construction5Vibrations and changes in water pressure experienced during construction can dislodge biofilm and free Legionella into the water entering the building. at hospitalLack of start-up and shutdown procedure for decorative fountainsDisinfectant not added to decorative fountain✔✔✔✔Long-term care facilityPotable waterTemperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in hot potable water (because of anti-scalding regulations)Thermostatic mixing valves placed nearer to hot water heater than to faucet, creating long lengths of piping with temperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F).Inadequate disinfectant in potable water✔Long-term care facilityPotable waterInadequate disinfectant in potable water✔Long-term care facilityCooling towerInadequate disinfectant in cooling tower because of timed delivery that did not allow disinfectant to be delivered when cooling tower was not running✔Senior living facilityPotable waterTemperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in hot potable water because of reduction of hot water heater from original temperature set by the building's contractorsExcessive sediment in potable water system because of new construction 5Vibrations and changes in water pressure experienced during construction can dislodge biofilm and free Legionella into the water entering the building.Broken water main5Vibrations and changes in water pressure experienced during construction can dislodge biofilm and free Legionella into the water entering the building. during construction5Vibrations and changes in water pressure experienced during construction can dislodge biofilm and free Legionella into the water entering the building.✔✔Senior living facilityPotable waterTemperatures in optimal range for Legionella growth2Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F). in hot potable waterInadequate disinfectant in potable waterFailure to follow manufacturer's recommendations for periodic draining of hot water heaters to remove sediment✔✔✔✔Water temperature in hot water heater lower than indicated on thermostatMaintenance of water main4Broken water mains lead to changes in water pressure which can dislodge biofilm (thereby freeing Legionella into water entering the building) and can introduce particulate matter into water entering the building (which can consume disinfectant). resulting in pressure disruptions and water outageCommunityCooling towerTropical storm with heavy rain and flooding immediately before symptom onset of first case6Investigators suspect inadequate maintenance of cooling towers (with inadequate disinfectant) a heavy rain.✔CommunityDecorative fountainInadequate maintenance of decorative fountain✔WorkplaceCooling towerLack of start-up and shutdown procedures for cooling towerLack of staff training on operation and maintenance of cooling towerCooling tower dysfunction, prompting opening of windowsHeavy rainfall, high humidity, and warm temperatures preceded onset of cases6Investigators suspect inadequate maintenance of cooling towers (with inadequate disinfectant) a heavy rain.✔✔✔Total1512881 Each reviewer independently assigned findings to one or more of four categories: (1) process failures, in which a process, such as a water management program, was missing or is inadequate; (2) human errors, in which a person did not perform as expected (e.g. not replacing hot tub filters according to manufacturer's recommendations); (3) equipment failures, in which a piece of equipment did not operate as expected (e.g. a malfunctioning disinfectant delivery system); and (4) unmanaged external changes, in which adjustments were not made to account for events outside a building water system (e.g. nearby construction leading to changes in potable water quality).2 Although recovery of Legionella from water with temperatures outside this range have occurred, the temperature range most favorable for growth of Legionella is 25°C–42°C (77°F–108°F). For health care facilities, ASHRAE Guideline 12-2000 recommends storing and distributing cold water at <20°C (68°F), whereas hot water should be stored at >60°C (140°F) and circulated with a minimum return temperature of 51°C (124°F). In other settings, hot water should be stored at =40°C (=120°F).3 Water stagnation encourages biofilm growth, reduces temperature, and reduces levels of disinfectant.4 Broken water mains lead to changes in water pressure which can dislodge biofilm (thereby freeing Legionella into water entering the building) and can introduce particulate matter into water entering the building (which can consume disinfectant).5 Vibrations and changes in water pressure experienced during construction can dislodge biofilm and free Legionella into the water entering the building.6 Investigators suspect inadequate maintenance of cooling towers (with inadequate disinfectant) a heavy rain. Open table in a new tab The number of cases of Legionnaires’ disease in the United States is increasing, and associated mortality is substantial. Identifying ways to reduce environmental transmission of Legionella is crucial to reducing morbidity and mortality associated with Legionnaires’ disease. The new ASHRAE standard establishes minimum requirements for management of the risk for Legionella growth and transmission in building water systems. Gaps in maintenance that could be addressed with a water management program to prevent Legionnaires’ disease outbreaks were described in 23 (85%) of 27 investigated outbreaks. Outbreaks resulted from a combination of deficiencies, most frequently classified as process failures and human errors. In the majority of outbreaks, inadequate water disinfectant levels and temperatures in the optimal range for Legionella growth were observed; implementing a functional water management program could address these deficiencies through routine monitoring of disinfectant levels and water temperature (10ASHRAE. Legionellosis: Risk management for building water systems. ANSI/ASHRAE Standard 188–2015. Atlanta, GA: ASHRAE; 2015. Available from: http://www.mesc.org/downloads/v/PCTI/ASHRAE%20188%20-%202015%20FINAL.pdf.Google Scholar). Deficiencies related to equipment failures and unmanaged external changes were less common but are also remediable through preventive measures, such as flushing of potable water systems after water main breaks. Although approximately half the outbreaks included in this analysis resulted from multiple deficiencies, approximately half resulted from a single deficiency, suggesting that even a single deficiency can be sufficient to cause an outbreak; thus, all deficiencies should be addressed.