Legionnaires’ Disease Outbreak Associated With a Hot Tub Display at the North Carolina Mountain State Fair, September 2019
Abstract
Objectives:
On September 23, 2019, the North Carolina Division of Public Health identified a legionellosis increase in western North Carolina; most patients had recently attended the North Carolina Mountain State Fair. We conducted a source investigation.
Methods:
Cases were fair attendees with laboratory-confirmed legionellosis and symptom onset within 2 to 14 days (Legionnaires’ disease) or ≤3 days (Pontiac fever). We conducted a case-control study matching cases to non-ill fair attendees as control participants and an environmental investigation, and we performed laboratory testing (Legionella bacteria culture and polymerase chain reaction) of 27 environmental samples from fairgrounds and hot tubs and 14 specimens from case patients. We used multivariable unconditional logistic regression models to calculate adjusted odds ratios for potential Legionella exposure sources and risk factors.
Results:
Of 136 people identified with fair-associated legionellosis, 98 (72%) were hospitalized and 4 (3%) died. Case patients were more likely than control participants to report walking by hot tub displays (adjusted odds ratio = 10.0; 95% CI, 4.2-24.1). Complete hot tub water treatment records were not kept, precluding evaluation of water maintenance conducted on display hot tubs. Legionella pneumophila sequence types (STs) were consistent among 10 typed clinical specimens (ST224) but distinct from the only positive environmental sample from the fair (ST7 and ST8).
Conclusions:
Hot tub displays were identified as the most likely outbreak source, making this the largest hot tub–associated Legionnaires’ disease outbreak worldwide. Following the investigation, the North Carolina Division of Public Health and the Centers for Disease Control and Prevention released guidance on mitigating risk of Legionella exposure from hot tub displays. Results highlight the importance of properly maintaining equipment that aerosolizes water, including hot tubs intended for display purposes only.
Keywords: Legionnaires’ disease, legionellosis, outbreak, spa, hot tub, fair
On September 23, 2019, the North Carolina Division of Public Health (NCDPH) was notified of an increase in legionellosis in Buncombe County and Henderson County: 13 people with Legionnaires’ disease reported attending the North Carolina Mountain State Fair, which ran September 6-15, 2019, at the Western North Carolina Agricultural Center (WNC Agricultural Center) in Fletcher, North Carolina (Buncombe County).
The fairgrounds and surrounding area were identified as a potential outbreak source. Patients and fair attendees reported that filled hot tubs were on display inside a building at the fairgrounds. Hot tub displays have been implicated previously as a source for Legionella infections.1 -5 In collaboration with local, state, and federal partners, NCDPH investigated the outbreak to determine the source and provide mitigation recommendations for similar settings. Here, we describe the epidemiology, environmental setting, and source investigation for a large outbreak of Legionnaires’ disease among attendees and workers at the Mountain State Fair in September 2019.
Methods
The Centers for Disease Control and Prevention (CDC) reviewed this activity and determined that it was conducted consistent with applicable federal law and CDC policy (eg, 45 CFR part 46; 21 CFR part 56; 42 USC §241[d]; 5 USC §552a; 44 USC §3501 et seq).
Case Definition
We classified a confirmed Legionnaires’ disease case as a patient with laboratory-confirmed Legionella infection, clinically or radiographically diagnosed pneumonia, and symptom onset 2 to 14 days after Mountain State Fair attendance. We classified a confirmed Pontiac fever case as a patient with laboratory-confirmed Legionella infection and symptoms of fever, myalgia, headache, chills, nausea, vomiting, or diarrhea ≤3 days after Mountain State Fair attendance but without clinically or radiographically confirmed pneumonia. We defined laboratory-confirmed Legionella infection as culture isolation, nucleic acid amplification test detection, or a positive urinary antigen test (UAT) result. We classified cases as suspected if they met the clinical criteria for outbreak-associated Legionnaires’ disease without laboratory confirmation of Legionella infection.
Case Finding and Analysis
NCDPH and CDC sent statewide and national health alerts, respectively, to physicians, public health practitioners, health care facilities, and media on September 24, 2019. NCDPH issued guidance to physicians on September 25, 2019, advising the use of UATs and sputum cultures to test for Legionella infection among patients who attended the Mountain State Fair and had symptoms compatible with Legionnaires’ disease or Pontiac fever. NCDPH also issued a statewide request for submission of clinical specimens to North Carolina hospital laboratories on September 27, 2019. We used a Pearson χ2 test (α = .05) to compare the proportion of people identified with legionellosis who attended the Mountain State Fair during September 11-15, 2019 (second half of the fair), with the proportion of total people who attended during that time, to assess whether risk differed over time.
Environmental Investigation
During September 25-27, 2019, NCDPH conducted a site visit to the WNC Agricultural Center with staff from the North Carolina Department of Agriculture and Consumer Services, Buncombe County Health and Human Services, and CDC to identify sources of aerosolized water present during the Mountain State Fair and to collect environmental samples. CDC assessed ventilation systems and air circulation patterns in buildings that housed potential sources of aerosolized water during the Mountain State Fair.
The Davis Event Center at the WNC Agricultural Center had 3 hot tubs on display during the Mountain State Fair. During the site visit at the Davis Event Center, we collected bulk water from indoor men’s and women’s restrooms (1 sample from each) and hose bibbs (n = 2); we also collected bulk water and a swab sample from 1 outdoor hose bibb and swab samples from an evaporative cooling fan (n = 5) used at the fair. We collected 14 swab samples from 3 hot tubs that were in use at the Mountain State Fair but stored off-site at the time of sampling and 2 hot tub filter samples (1 in use at the fair and 1 new filter that was in the hot tub at the time of sampling). Of the sampled hot tubs, we were not able to access 2 hot tubs until October 7, 2019. All hot tubs had been drained, cleaned, and dried before sampling.
Laboratory Investigation
NCDPH submitted all clinical specimens and environmental samples (n = 27 bulk water and swabs) to CDC for culture and other testing, according to previously established methods. 6 CDC screened clinical and environmental isolates with a multiplex polymerase chain reaction assay to test for Legionella pneumophila serogroup 1. 7 CDC used next-generation sequencing methods to characterize the genomes of all clinical isolates and representative environmental isolates determined to be L pneumophila serogroup 1. 8 We also used nested sequence-based typing, according to the methods of the European Study Group for Legionella Infections, to derive culture-independent typing information from some clinical specimens that did not yield isolates.9,10 We measured temperature, pH, and free Cl2 (mg/L) for all bulk water samples taken from the WNC Agricultural Center. We used Spartan Cube (Spartan Bioscience Inc) polymerase chain reaction testing on 3 swab samples from 1 hot tub to test for the presence of L pneumophila. 11
Case-Control Study
NCDPH conducted a case-control study to identify potential sources of Legionella exposure and behaviors associated with infection. We invited Mountain State Fair attendees and workers to participate in the study if they had illnesses meeting the confirmed case definition and that were reported to NCDPH by October 1, 2019. NCDPH sent a case patient survey that asked about activities and places visited at the Mountain State Fair and risk factors for Legionnaires’ disease.
We used a 2-stage selection process to identify potential control participants who attended the Mountain State Fair in 2019. For stage 1, we sent an online screening survey to fair attendees who purchased online tickets, fair vendors, and employees of the North Carolina Department of Agriculture and Consumer Services who worked at the Mountain State Fair in 2019. Local media in western North Carolina advertised the stage 1 survey, and recipients were able to forward the survey to other Mountain State Fair attendees. From stage 1 survey respondents, we selected 2.5 frequency age-matched control participants who were not ill after the fair for each case patient respondent by randomly ordering a list of eligible control participants for each age group and selecting them in order until the target number was reached. We sent the stage 2 survey to all selected people in the control group; the control survey had questions similar to the survey for case patients. We used Survey Monkey (Momentive) for online surveys. We collected information about dates of attendance, places visited at the Mountain State Fair (including amount of time spent in specific areas), instances of visiting or seeing identified sources of aerosolized water, and information on known risk factors for Legionnaires’ disease. 12
Statistical Analysis
We used separate multivariable unconditional logistic regression models adjusted for age and gender to calculate adjusted odds ratios (aORs) and 95% CIs for each exposure among case patients and control participants. For models with limited cell size (<5), we used exact logistic regression. We compared distributions of last date of Mountain State Fair attendance among case patients and control participants using a Mann–Whitney U test. We compared proportions and means between survey respondents and nonrespondents using Pearson χ2 tests and t tests, respectively. We used SAS version 9.4 (SAS Institute, Inc) for all statistical analyses.
Results
Epidemiologic Investigation
We identified 136 patients with confirmed legionellosis (135 with Legionnaires’ disease and 1 with Pontiac fever) and 35 patients with suspected Legionnaires’ disease who attended the Mountain State Fair. Of 136 patients with confirmed legionellosis, 133 had positive UAT results, 1 had a positive culture result, and 2 had positive nucleic acid amplification test results. Suspected cases met the clinical definition but did not meet the confirmatory laboratory criteria: among 35 suspected cases, 19 had negative UAT results, 4 had single-antibody serologies, and 12 had no laboratory results.
Patients with confirmed infection resided in 17 North Carolina counties and 4 other states; most were tested (74 of 135; 55%) and reported to public health departments (116 of 134; 87%) after the release of a health alert and press communication from NCDPH on September 24, 2019 (Figure 1). Patients with confirmed infection ranged in age from 24 to 91 (median, 61), and most were White (79%) and men (57%). Of those who reported an ethnicity (n = 103), all identified as non-Hispanic. Among patients with confirmed Legionnaires’ disease, 98 (73%) were hospitalized and 4 (3%) died. The date range of symptom onset in confirmed cases was September 13-27, 2019 (Figure 1). Among 69 patients with confirmed Legionnaires’ disease, a recorded symptom-onset date, and only 1 day of Mountain State Fair attendance, the incubation period was 3 to 11 days, with a median (IQR) of 6 (5-8) days.
Figure 1.
Confirmed cases of legionellosis associated with the North Carolina Mountain State Fair, September 6-15, 2019. Cases are shown by date of visit, symptom-onset date, testing date, and date of report to public health. The North Carolina Division of Public Health was notified about a cluster of cases in western North Carolina on September 23, 2019. A health alert was issued on September 24, 2019, to physicians, public health practitioners, health care facilities, and media. The blue line represents the fair attendance date. Because many case patients attended the fair on multiple days, individuals represented on the blue line may contribute to >1 date. One case patient from out of state was missing a testing date. An additional 5 case patients were reported to public health departments during October 7-26, 2019, and are not shown, and 2 case patients are missing date of report to the public health department. Data source: North Carolina Division of Public Health.
Of 135 patients with confirmed Legionnaires’ disease, 122 (90%) had ≥1 underlying condition or risk factor for Legionnaires’ disease. Specifically, 106 (79%) were aged >50 years; 40 (30%) were smokers or had chronic lung disease; 21 (16%) had an immunosuppressive condition; 14 (10%) had a malignancy; 12 (9%) had kidney disease; 11 (8%) were undergoing an immunosuppressive therapy; and 4 (3%) had liver disease. Among hospitalized patients, 91 (93%) had ≥1 underlying condition or risk factor for Legionnaires’ disease.
The Mountain State Fair had an attendance of 171 361 people, with the highest attendance on the first and last weekends (September 6-8 and 13-15). Patients with confirmed legionellosis attended or worked at the Mountain State Fair during September 5-19, 2019, for 223 patient fair-visit days (some workers were there longer to set up and take down displays); 69% of those visits occurred during the second half of the fair (Figure 1). The proportion of patient fair-visit days during the second half was significantly different (P < .001) from that of the total Mountain State Fair attendance (51%) during the same period. Among 102 patients with confirmed Legionnaires’ disease who reported duration of attendance, the median number of days attending the fair was 1 day (range, 1-11 d).
Environmental Investigation
Potential sources of aerosolized water at the Mountain State Fair included hot tubs and diffusers on display in the Davis Event Center, an evaporative cooling fan, rides involving water, and hoses for dust reduction. Complete hot tub maintenance records were not kept by vendors, precluding determination of whether the water in the hot tubs was properly maintained during the fair.
The Davis Event Center is a 4180-m2 building with a high-efficiency ventilation system that altered outdoor air exchange based on the outdoor temperature. Because of high temperatures during the Mountain State Fair (average daily temperature, 21 °C to 24 °C; maximum daily temperature, 28 °C to 33 °C), outdoor air exchange was reduced and air inside the building had increased recirculation. Air inside the building was further recirculated by high-volume, low-speed ceiling fans. This system distributed air from the main hall into the café and restrooms, which were in the building but separated from the main exhibit hall by doors.
Laboratory Findings
Lower respiratory specimens were obtained from 14 patients. L pneumophila was isolated from 10 specimens: 5 with a full sequence–based typing profile of sequence type (ST) 224 and 5 with partial profiles that were consistent with ST224. Among the 27 bulk water and environmental swabs, only 1 bulk water sample from the women’s restroom at the Davis Event Center had positive culture results for L pneumophila serogroup 1. This sample yielded 2 isolates of closely related STs, ST7 and ST8, which are relatively common in the environment. ST7 and ST8 share 6 of 7 alleles in the sequence-based typing profile and are more closely related to each other than ST224, which shares 0 of 7 alleles with either ST7 or ST8.
Additional test results of 5 bulk water samples yielded free Cl2 ranging from 0.00 mg/L (outside hose bibb) to 0.92 mg/L (men’s restroom water heater), probe pH from 6.53 (women’s restroom sink) to 9.10 (men’s restroom water heater), and temperatures from 21.1 °C (men’s restroom water heater) to 24.4 °C (women’s restroom and indoor hose bibb).
Participants in the Case-Control Study
By October 1, 2019, 95 Mountain State Fair attendees with confirmed legionellosis were reported to the state and invited to participate in the case-control study. Surveys were completed by 57 (60%) confirmed case patients. Among case patients, survey respondents and nonrespondents did not differ significantly by age (P = .56), gender (P = .99), race (P = .44), ethnicity (P = .61), or hospitalization status (P = .40).
Stage 1 surveys for the control group were sent to 2729 fairgoers; after wider distribution, 7588 people responded. Stage 2 surveys were sent to 243 randomly selected eligible age-matched respondents to the stage 1 survey; 138 (57%) responded and were enrolled as control participants (Figure 2). Among control participants, no significant difference in response rate by age group was reported (P = .40).
Figure 2.
Case patients and control participants included in the North Carolina Mountain State Fair Legionnaires’ disease investigation, September 2019. Eligible control participants were attendees who did not get sick after the fair, provided an age, and agreed to be contacted again. Data source: North Carolina Division of Public Health.
Most case patients were aged ≥60 years (60%), and a significantly greater proportion of case patients (61%) than control participants (38%) were male (P = .002). Approximately 90% of case patients and control participants resided in North Carolina; 21% of case patients and 25% of control participants were Mountain State Fair workers (Table 1).
Table 1.
Characteristics of participants in a case-control study to investigate the source of a legionellosis outbreak at the North Carolina Mountain State Fair, September 6-15, 2019 a
Characteristic | Case patients (n = 57) | Control participants (n = 138) |
---|---|---|
Age, y | ||
0-39 | 3 (5) | 3 (2) |
40-49 | 11 (19) | 26 (19) |
50-59 | 9 (16) | 32 (23) |
60-69 | 14 (25) | 31 (22) |
≥70 | 20 (35) | 46 (33) |
Gender | ||
Male | 35 (61) | 52 (38) |
Female | 22 (39) | 86 (63) |
State of residence | ||
North Carolina | 53 (93) | 126 (91) |
Outside North Carolina | 4 (7) | 12 (9) |
Type of attendance b | ||
Visitor | 47 (82) | 107 (78) |
Worker | 12 (21) | 34 (25) |
Case-Control Study Risk Factor Analysis
Exposures associated with legionellosis included the following: visiting the Davis Event Center (aOR = 10.6; 95% CI, 3.0-58.6), Virginia Boone building (aOR = 2.8; 95% CI, 1.4-5.5), Heritage exhibits (aOR = 2.6; 95% CI, 1.3-5.3), or Expo Center (aOR = 2.4; 95% CI, 1.2-4.7); walking by or spending time at the hot tubs (aOR = 10.1; 95% CI, 4.2-24.2); seeing the diffuser display in the Davis Event Center (aOR = 7.4; 95% CI, 2.9-19.1); and spending time at (aOR = 6.6; 95% CI, 1.3-44.0) or seeing (aOR = 3.2; 95% CI, 1.4-7.5) the evaporative cooling fan by the first aid station. Visiting the Mountain State Fair during September 12-15 (aOR = 24.2; 95% CI, 6.9-132.5) and spending >1 hour in the Davis Event Center (aOR = 18.5; 95% CI, 4.7-110.8) also increased odds of legionellosis (Table 2). When we included people in the analysis who went only into the restrooms or café (both of which could be entered without going through the main hall), we found that 100% of case patients, compared with 72% of control participants, entered the Davis Event Center.
Table 2.
Multivariable analysis of exposures and risk factors for legionellosis among North Carolina Mountain State Fair attendees, September 6-15, 2019, who participated in a case-control study a
Exposure | Case patients (n = 57) | Control participants (n = 138) | Missing | Adjusted OR (95% CI) b |
---|---|---|---|---|
Date of fair attendance (N = 194) | ||||
Attendance during September 12-15 | 54 | 62 | 0 | 24.2 (6.9-132.5) c |
Davis Event Center | ||||
Any Davis Event Center visit (including restroom or café) | 57 | 99 | Not available d | |
Reported entering the Davis Event Center | 54 | 91 | 0 | 10.6 (3.0-58.6) c |
Davis Event Center restroom | 40 | 74 | 2 | 2.5 (1.2-5.0) |
Went into or sat down in café | 14 | 17 | 2 | 2.7 (1.2-6.4) |
Time spent in the Davis Event Center, h | ||||
0 | 3 | 47 | 13 | 1 [Reference] |
≤1 | 26 | 58 | 13 | 7.7 (2.1-44.3) c |
>1 | 25 | 23 | 13 | 18.5 (4.7-110.8) c |
Hot tub | ||||
Walked by or spent time | 47 | 56 | 3 | 10.1 (4.2-24.2) |
Walked by | 47 | 56 | 4 | 10.0 (4.2-24.1) |
Spent time | 14 | 13 | 3 | 4.2 (1.7-10.4) |
Area of fair | ||||
Expo Center | 40 | 73 | 0 | 2.4 (1.2-4.7) |
Virginia Boone building | 38 | 62 | 0 | 2.8 (1.4-5.5) |
Animal barns | 29 | 82 | 0 | 0.7 (0.4-1.4) |
Animal exhibits | 21 | 50 | 0 | 1.0 (0.5-2.0) |
Heritage exhibits | 27 | 44 | 0 | 2.6 (1.3-5.3) |
Midway | 37 | 109 | 0 | 0.5 (0.2-1.1) |
First aid station | 4 | 5 | 0 | 1.8 (0.3-8.8) |
First aid station evaporative cooling fan | ||||
Saw fan | 15 | 14 | 6 | 3.2 (1.4-7.5) |
Spent time or felt water | 6 | 3 | 6 | 6.6 (1.3-44.0) c |
Other fans blowing mist | ||||
Walked by fans blowing mist | 9 | 13 | 6 | 1.9 (0.8-5.0) |
Diffuser display | ||||
Saw diffusers | 17 | 9 | 4 | 7.4 (2.9-19.1) |
Spent time looking at diffusers | 5 | 2 | 4 | 7.3 (1.0-86.1) c |
Risk factors | ||||
Smoking | ||||
Current smoker/vaper | 3 | 7 | 3 | 1.6 (0.2-8.4) c |
Former smoker/vaper | 13 | 35 | 3 | 0.8 (0.3-1.7) |
Medical treatment | ||||
None | 30 | 120 | 10 | 0.2 (0.1-0.4) |
Nebulizer | 4 | 2 | 10 | 5.8 (0.8-68.0) c |
CPAP | 8 | 11 | 10 | 1.6 (0.6-4.4) |
Supplemental oxygen | 9 | 3 | 10 | 8.5 (1.9-52.2) c |
Immunosuppressants | 5 | 3 | 10 | 6.9 (1.2-49.5) c |
Predisposing condition | ||||
None | 32 | 101 | 3 | 0.4 (0.2-0.8) |
Diabetes | 11 | 14 | 3 | 2.4 (1.0-5.9) |
Cancer | 12 | 16 | 3 | 2.5 (1.0-6.1) |
Liver disease | 2 | 0 | 3 | Undefined |
Kidney disease | 3 | 3 | 3 | 1.8 (0.2-15.0) c |
Chronic lung disease | 3 | 6 | 3 | 1.5 (0.2-7.7) c |
We observed a significant difference in the distribution of last date of Mountain State Fair attendance between case patients and control participants. Last dates of attendance for case patients occurred September 10-15, whereas those for control participants occurred September 6-15 (P < .001) (Figure 3).
Figure 3.
Case patients and control participants included in the North Carolina Mountain State Fair Legionnaires’ disease investigation, by last date of attendance at the North Carolina Mountain State Fair, September 6-15, 2019. Data source: North Carolina Division of Public Health.
Other risk factors that showed a significant association with legionellosis included use of immunosuppressants or supplemental oxygen, presence of diabetes, and presence of cancer. Smoking or vaping was not associated with increased odds of legionellosis (Table 2).
Discussion
Results of the case-control study and environmental investigation indicated that the outbreak source was most likely hot tubs on display in the Davis Event Center. Our case-control study showed that the strongest exposure associations with legionellosis were entering the Davis Event Center, Mountain State Fair attendance during September 12-15, spending >1 hour in the Davis Event Center, and walking by or spending time near the hot tubs.
Hot tubs are a well-established source of aerosolized water exposure and have been associated with previous outbreaks of Legionnaires’ disease13 -16 and Pontiac fever17 -20 nationally and internationally. Display hot tubs have been associated with multiple previous outbreaks, including a flower show in the Netherlands (133 cases) 1 and retail outlets in Virginia (23 cases), 2 the United Kingdom (4 of 21 cases),3,4 and New Zealand (3 cases). 5 Although the environmental isolates did not match the clinical isolates genetically, the presence of L pneumophila in a bulk water sample from the Davis Event Center indicates that L pneumophila may have been introduced into the hot tubs from the fairgrounds when they were filled, and conditions during the Mountain State Fair may have allowed for the growth of L pneumophila ST224. Alternatively, L pneumophila ST224 may have been present in the hot tubs before they were filled, with presence then amplified during the fair. This study underscores the importance of collecting environmental samples as soon as possible and before cleaning or disinfecting the suspected sources.
The timing of Mountain State Fair attendance among case patients and control participants supports the possibility that L pneumophila was amplified in hot tubs during the fair. Almost all case patients (95%) attended the fair September 12-15, 2019. The increased odds of infection later in the fair indicate that levels of L pneumophila in the hot tubs likely increased over time. Legionella pneumophila can thrive in warm freshwater environments where disinfectant levels are low or not properly maintained. 21 Hot tubs are often heated to 38 °C to 40 °C, whereas Legionella grows best at 25 °C to 45 °C. 22 After the bacteria grow to sufficient numbers, they can infect people who inhale the mist. 23 The warm and possibly improperly maintained environment in the hot tubs likely allowed for proliferation of L pneumophila to a level sufficient to infect many people.
Other exposures that showed significant, although weaker, effects were not considered likely outbreak sources, including exposure to the evaporative cooling fan, the diffuser display, the Expo Center, the Virginia Boone building, and the Heritage exhibits. All of these showed a positive association with infection; however, aORs for these exposure areas were lower than for the Davis Event Center, and fewer case patients went in or near these areas than in the Davis Event Center. No significant sources of aerosolized water were identified in these locations, aside from the evaporative cooling fan, where only 6 case patients reported spending time.
To the best of our knowledge, this outbreak of Legionnaires’ disease was among the largest in the United States and was the largest hot tub–associated outbreak reported worldwide. The largest previous hot tub–associated outbreak reported 133 confirmed cases associated with a flower show in the Netherlands. 1 At the Mountain State Fair, the large volume of fair attendees, the likely concentration of aerosolized L pneumophila in the hot tubs for multiple days, and the dispersion of the aerosols throughout the building by high-volume, low-speed fans resulted in many exposed individuals.
Despite the large outbreak at the Mountain State Fair, the mortality rate was 3%. Mortality for other community-acquired Legionnaires’ disease outbreaks has ranged from 1% 24 to approximately 10%.1,25 Mortality may have been mitigated by the quick public health response, notification of health care providers, and widespread media coverage. Knowledgeable health care providers were likely to have been quick to test, diagnose, and initiate treatment for Legionnaires’ disease. Likewise, media coverage might have prompted individuals who went to the Mountain State Fair and became sick to promptly seek health care services and treatment.
Given the magnitude of the outbreak and previous evidence of risk of Legionella exposure from hot tub displays, further public health action on hot tub displays is warranted. Large state fairs and similar events are popular places for hot tub vendors.26,27 On September 25, 2019, NCDPH released new guidance for temporary event vendors about the safe display of hot tubs and other misting equipment. 28 In November 2019, CDC released a health advisory with updated guidance for environmental and public health practitioners on minimizing risks from hot tub displays at temporary events such as fairs. 29 In July 2021, North Carolina added “spas operating for display at temporary events” to section 130A-280 of the general statute, requiring that hot tubs on display be regulated for the protection of public health, similar to public swimming pools and spas. 30
Limitations
This study had at least 3 limitations. First, samples were not collected from hot tubs until 12 to 22 days after the Mountain State Fair, after hot tubs had been cleaned and dried. This delay limited the possibility of obtaining a positive culture and precluded comparison of clinical specimens with environmental isolates obtained from the suspected source. Second, incomplete recordkeeping prevented review of hot tub water maintenance conducted during the Mountain State Fair; thus, water treatment practices, such as incomplete chlorination or system flushing, that may have permitted amplification of L pneumophila could not be determined. 28 Third, the response rate for the case-control study was about 60% for both case patients and control participants. However, for variables that were assessed (demographic characteristics and hospitalization rates among case patients; age among control participants), we found no significant differences between respondents and nonrespondents.
Conclusions
A rapid public health investigation determined that hot tubs on display at the North Carolina Mountain State Fair were the likely source of a large outbreak of Legionnaires’ disease. Our outbreak investigation highlights the importance of properly maintaining all equipment that aerosolizes water, including hot tubs intended for display purposes only.
Acknowledgments
We thank those who supported work on this investigation, including Veronica Bryant, MPH, Evelyn Foust, MPH, Vanessa M. Gailor, BSN, RN, Molly Hoffman, MPH, Nicole Lee, MPH, James Lewis, MD, MPH, Anita Valiani, MPH, and Carl Williams, DVM, from the North Carolina Division of Public Health; Stacey Bosch, DVM, MPH, from the Centers for Disease Control and Prevention; and Jan Shepard, MBA, from Buncombe County Health and Human Services. We also appreciate collaboration with the following investigative partners: North Carolina Department of Agriculture and Consumer Services, Buncombe County Health and Human Services, and the Henderson County Department of Public Health.
Footnotes
Disclaimer: The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The authors received no financial support for the research, authorship, and/or publication of this article.
References
- 1. Den Boer JW, Yzerman EPF, Schellekens J, et al. A large outbreak of Legionnaires’ disease at a flower show, the Netherlands, 1999. Emerg Infect Dis. 2002;8(1):37-43. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Benkel DH, McClure EM, Woolard D, et al. Outbreak of Legionnaires’ disease associated with a display whirlpool spa. Int J Epidemiol. 2000;29(6):1092-1098. doi: 10.1093/ije/29.6.1092 [DOI] [PubMed] [Google Scholar]
- 3. McEvoy M, Batchelor N, Hamilton G, et al. A cluster of cases of Legionnaires’ disease associated with exposure to a spa pool on display. Commun Dis Public Health. 2000;3(1):43-45. [PubMed] [Google Scholar]
- 4. Coetzee N, Duggal H, Hawker J, et al. An outbreak of Legionnaires’ disease associated with a display spa pool in retail premises, Stoke-on-Trent, United Kingdom, July 2012. Euro Surveill. 2012;17(37):20271. [PubMed] [Google Scholar]
- 5. Ruscoe Q, Hill S, Blackmore T, McLean M. An outbreak of Legionella pneumophila suspected to be associated with spa pools on display at a retail store in New Zealand. N Z Med J. 2006;119(1243):U2253. [PubMed] [Google Scholar]
- 6. Kozak-Muiznieks NA, Lucas CE, Brown E, et al. Prevalence of sequence types among clinical and environmental isolates of Legionella pneumophila serogroup 1 in the United States from 1982 to 2012. J Clin Microbiol. 2014;52(1):201-211. doi: 10.1128/JCM.01973-13 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Benitez AJ, Winchell JM. Clinical application of a multiplex real-time PCR assay for simultaneous detection of Legionella species, Legionella pneumophila, and Legionella pneumophila serogroup 1. J Clin Microbiol. 2013;51(1):348-351. doi: 10.1128/JCM.02510-12 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Raphael BH, Baker DJ, Nazarian E, et al. Genomic resolution of outbreak-associated Legionella pneumophila serogroup 1 isolates from New York State. Appl Environ Microbiol. 2016;82(12):3582-3590. doi: 10.1128/AEM.00362-16 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Gaia V, Fry NK, Harrison TG, Peduzzi R. Sequence-based typing of Legionella pneumophila serogroup 1 offers the potential for true portability in legionellosis outbreak investigation. J Clin Microbiol. 2003;41(7):2932-2939. doi: 10.1128/JCM.41.7.2932-2939.2003 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Ratzow S, Gaia V, Helbig JH, Fry NK, Lück PC. Addition of neuA, the gene encoding N-acylneuraminate cytidylyl transferase, increases the discriminatory ability of the consensus sequence-based scheme for typing Legionella pneumophila serogroup 1 strains. J Clin Microbiol. 2007;45(6):1965-1968. doi: 10.1128/JCM.00261-07 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Ahmed S, Liwak-Muir U, Walker D, et al. Validation and in-field testing of a new on-site qPCR system for quantification of Legionella pneumophila according to ISO/TS 12869:2012 in HVAC cooling towers. J Water Health. 2019;17(2):237-253. doi: 10.2166/wh.2019.252 [DOI] [PubMed] [Google Scholar]
- 12. North Carolina Department of Health and Human Services. Legionnaires’ disease outbreak associated with the North Carolina Mountain State Fair, 2019. Accessed June 15, 2021. https://epi.dph.ncdhhs.gov/cd/legionellosis/MSFOutbreakReport_FINAL.pdf?ver=1.1 [DOI] [PMC free article] [PubMed]
- 13. Spitalny KC, Vogt RL, Witherell LE. National survey on outbreaks associated with whirlpool spas. Am J Public Health. 1984;74(7):725-726. doi: 10.2105/ajph.74.7.725 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Vogt RL, Hudson PJ, Orciari L, Heun EM, Woods TC. Legionnaires’ disease and a whirlpool-spa. Ann Intern Med. 1987;107(4):596. doi: 10.7326/0003-4819-107-4-596_1 [DOI] [PubMed] [Google Scholar]
- 15. Jernigan DB, Hofmann J, Cetron MS, et al. Outbreak of Legionnaires’ disease among cruise ship passengers exposed to a contaminated whirlpool spa. Lancet. 1996;347(9000):494-499. doi: 10.1016/s0140-6736(96)91137-x [DOI] [PubMed] [Google Scholar]
- 16. Centers for Disease Control and Prevention. Legionnaires disease associated with a whirlpool spa display—Virginia, September–October, 1996. MMWR Morb Mortal Wkly Rep. 1997;46(4):83-86. [PubMed] [Google Scholar]
- 17. Spitalny KC, Vogt RL, Orciari LA, Witherell LE, Etkind P, Novick LF. Pontiac fever associated with a whirlpool spa. Am J Epidemiol. 1984;120(6):809-817. doi: 10.1093/oxfordjournals.aje.a113953 [DOI] [PubMed] [Google Scholar]
- 18. Fallon RJ, Rowbotham TJ. Microbiological investigations into an outbreak of Pontiac fever due to Legionella micdadei associated with use of a whirlpool. J Clin Pathol. 1990;43(6):479-483. doi: 10.1136/jcp.43.6.479 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19. Mangione EJ, Remis RS, Tait KA, et al. An outbreak of Pontiac fever related to whirlpool use, Michigan 1982. JAMA. 1985;253(4):535-539. [PubMed] [Google Scholar]
- 20. Lüttichau HR, Vinther C, Uldum SA, Møller J, Faber M, Jensen JS. An outbreak of Pontiac fever among children following use of a whirlpool. Clin Infect Dis. 1998;26(6):1374-1378. doi: 10.1086/516354 [DOI] [PubMed] [Google Scholar]
- 21. Garrison LE, Kunz JM, Cooley LA, et al. Vital signs: deficiencies in environmental control identified in outbreaks of Legionnaires’ disease—North America, 2000-2014. MMWR Morb Mortal Wkly Rep. 2016;65(22):576-584. doi: 10.15585/mmwr.mm6522e1 [DOI] [PubMed] [Google Scholar]
- 22. Centers for Disease Control and Prevention. What owners and managers of buildings and healthcare facilities need to know about the growth and spread of Legionella. Accessed August 5, 2021. https://www.cdc.gov/legionella/wmp/overview/growth-and-spread.html
- 23. Hunter CM, Laco J, Kunz J. Reducing Legionnaires’ disease in public spas. ASHRAE J. 2017;59:56-58. [PMC free article] [PubMed] [Google Scholar]
- 24. García-Fulgueiras A, Navarro C, Fenoll D, et al. Legionnaires’ disease outbreak in Murcia, Spain. Emerg Infect Dis. 2003;9(8):915-921. doi: 10.3201/eid0908.030337 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Lapierre P, Nazarian E, Zhu Y, et al. Legionnaires’ disease outbreak caused by endemic strain of Legionella pneumophila, New York, New York, USA, 2015. Emerg Infect Dis. 2017;23(11):1784-1791. doi: 10.3201/eid2311.170308 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. Hammell C. State fair hot tub sales: how to win big. Aqua Magazine. April 12, 2016. Accessed June 15, 2021. https://aquamagazine.com/retail/a-fair-advantage.html
- 27. Hot Tub Insider. The top 10 largest state fairs to buy a hot tub. Accessed June 15, 2021. https://hottubinsider.com/top-10-largest-state-fairs-buy-hot-tub
- 28. North Carolina Department of Health and Human Services. Legionellosis risk mitigation for temporary event vendors. September 25, 2019. Accessed June 15, 2021. https://epi.dph.ncdhhs.gov/cd/docs/LegionellaTemporaryFactSheet25Sep19.pdf
- 29. Centers for Disease Control and Prevention. Hot tub displays and Legionella risk—guidance for environmental and public health practitioners. March 25, 2020. Accessed June 15, 2021. https://www.cdc.gov/nceh/ehs/docs/factsheets/hot-tub-displays-ld-risk-p.pdf
- 30. North Carolina General Stat §130A-280 (2021). [Google Scholar]