Required water temperature in hotel plumbing to control Legionella growth

Highlights

• A systematic review of the association between temperature and Legionella in hotels.

• The effects of temperature to control Legionella were identified.

• 55 °C to 59 °C was identified as likely to reduce Legionella to non-detectable levels.

• Species of Legionella has a minimal impact, but analytical method affects results.

• Identified temperature can be used to calculate the water heater temperature.

Abstract

Legionella spp. occurring in hotel hot water systems, in particular Legionella pneumophila, are causing serious pneumonic infections, and water temperature is a key factor to control their occurrence in plumbing systems. We performed a systematic review and meta-analyses of the available evidence on the association between water temperature and Legionella colonization to identify the water temperature in hotel hot water systems required for control of Legionella. Qualitative synthesis and quantitative analysis were performed on 13 studies that met our inclusion criteria to identify the effect of temperature. The Receiver Operating Characteristic (ROC) curve identified 55 °C as a cutoff point for hotel hot water temperature with an Area Under the Curve (AUC) value of 0.914. The odds ratios (OR) for detecting Legionella at temperatures >55 °C compared to lower temperatures from a meta-analysis of three studies was 0.17 [95% CI: 0.11, 0.25], which indicates a strong negative association between temperature and Legionella colonization. A logistic regression on results from multiple studies using both molecular and culture methods found a temperature of 59 °C associated with an 8% probability of detectable Legionella. Only two studies reported sufficiently detailed data to allow a model of concentration vs. temperature to be fit, and this model was not statistically significant. Additional research or more detailed reporting of existing datasets is required to assess if Legionella growth can be limited below particular concentration targets at different temperatures.

Introduction

A number of opportunistic premise plumbing pathogens, including Legionella spp. can grow in building plumbing and pose a serious public health risk (Fraser et al., 1977; Rakic et al., 2013; Shands et al., 1985). Legionella spp. are gram-negative aerobic bacilli that can be found both in the natural and man-made aquatic environments (Fliermans et al., 1981; Fraser et al., 1977; Shands et al., 1985). Legionnaires’ disease (LD) and Pontiac fever, a pneumonia-type illness and mild flu-like illness, respectively, are caused by the inhalation of Legionella containing aerosols generated by taps, showers, spa waters, water fountains, cooling towers, etc. (Cordes and Fraser, 1980; Leoni et al., 2005; Shands et al., 1985, for a recent review of outbreaks and attributed causes see Hamilton et al., 2018). Previous studies have found that people at higher risk of getting LD include the elderly, smokers, cancer patients, diabetes patients, and immunosuppressed individuals (Bartram et al., 2007; Cordes and Fraser, 1980; Meenhorst et al., 1985). Presently, there are at least 60 species of Legionella, and at least 80 serogroups present in the environment (Benson and Fields, 1998; Brenner et al., 1979; Fields et al., 2002; Miyashita et al., 2020), but only a few of these have been related to legionellosis, such as Legionella pneumophila and Legionella micdadei (Cordes and Fraser, 1980; Dowling et al., 1984; Reingold et al., 1984). All the species of Legionella are not equally responsible for the Legionnaires’ disease, as L. pneumophila is by far the major cause of the disease (Fields et al., 2002; Mondino et al., 2020; Yu et al., 2002) and accounts for about 90% of the laboratory-confirmed cases in the United States and Europe (Yu et al., 2002).

Most of the LD cases are sporadic and community-acquired (about 69%), with smaller fractions that are travel-related and healthcare-related, which represent about 21% and 8% of total LD cases, respectively (European Centre for Disease Prevention and Control (ECDC), 2019; Yu et al., 2002). Premise plumbing systems in hospitals and hotels are a major source of Legionella infection (Cordes, 1981; Cordes and Fraser, 1980; Stout et al., 1985). Travel-related LD cases are often associated with Legionella transmission in hotels (Cowgill et al., 2005), and hot water systems are more likely to be colonized than cold water (Mouchtouri et al., 2007a). Cases of travel-associated Legionnaires’ disease were reported in more than 20 European countries and most of these cases (i.e., about 66%) were from the United Kingdom, Italy, France, and the Netherlands (ECDC, 2017a). Travel associated cases were also reported in the USA (Ahmed et al., 2019; Centers for Disease Control and Prevention (CDC), 2007; Cowgill et al., 2005; ECDC, 2017a), Canada and Australia (Environmental Protection Agency (EPA), 1999; Tobin, 1986). Fig. 1 shows the hotel and non-hotel-associated LD reported in Europe from 2000 to 2010. Between 2000 and 2010, out of a total of 7974 reported travel-associated Legionnaires’ disease, 7869 cases were hotel-associated which represent about 99% of the reported travel-associated cases (Jong et al., 2013; Joseph et al., 2009, Joseph et al., 2010; Lever et al., 2003; Mouchtouri and Rudge, 2015; Ricketts et al., 2010, 2008, 2007, 2006; Ricketts and Joseph, 2004a, 2004b).

Previous studies have explored the association between Legionella colonization and physio-chemical parameters of hotel water systems (Borella et al., 2005; Dennis et al., 1984; Groothuis et al., 1985; Kyritsi et al., 2018; Mouchtouri et al., 2007b), and the temperature was identified as a major factor for Legionella contamination in hotel hot water systems (Barna et al., 2016; Dennis et al., 1984; Groothuis et al., 1985; Mouchtouri et al., 2007b; Serrano-Suárez et al., 2013). Legionella spp. grows best in warm water, and many LD outbreaks are associated with hot water systems (Barna et al., 2016; Serrano-Suárez et al., 2013). Previous studies also found that many Legionella spp. including L. pneumophila, can even multiply at temperatures below 20 °C (Bartram et al., 2007; Söderberg et al., 2004). Legionella, in particular Legionella pneumophila, proliferates at water temperatures ranging between 20 and 45 °C with some studies reporting an optimum growth temperature of 35 °C (Alary and Joly, 1992; Bartram et al., 2007; Katz and Hammel, 1987) and other studies reporting an optimum growth temperature ≥ 37 °C (van der Kooij et al., 2016; Yee and Wadowsky, 1982). Previous studies have also found that they can survive for several hours at 50 °C (Bartram et al., 2007; Dennis et al., 1984; Schulze-Röbbecke et al., 1987), can remain viable at 60 °C for several minutes (Leoni et al., 2005) and can even survive a heat shock treatment of 70 °C for 30 min (Allegra et al., 2011). Hot water temperature in the plumbing system has been identified as an important factor to control Legionella growth in both published literature and guidance documents (Dennis et al., 1984, 1982; ECDC, 2017b; Groothuis et al., 1985; Montagna et al., 2018; Singh et al., 2020; See Rakic et al., 2013 for the contamination of Legionella pneumophila in water distribution systems and their associated factors). While temperature influences the growth of Legionella most, other factors such as disinfection efficiency, rate of corrosion, and the hydraulics of the plumbing systems also influence the survival and proliferation of Legionella spp. in premise plumbing systems (Lin et al., 1998; Shands et al., 1985; Stout et al., 1985; Singh et al., 2020).

The temperature in hotel hot water systems has an inverse association with Legionella colonization and can be used to control the system contamination (Dennis et al., 1984; Groothuis et al., 1985; Mouchtouri et al., 2007b; Rakic et al., 2013; Rakić et al., 2011; Yee and Wadowsky, 1982). The published literature has been inconsistent, with some studies suggesting maintaining hot water temperature ≥55 °C in hot water systems to control Legionella was required (Bargellini et al., 2011; Barna et al., 2016; Borella et al., 2005; Dennis et al., 1984; Mavridou et al., 1994; Toyosada et al., 2017; van der Lugt et al., 2019) while others suggesting ≥50 °C was enough (Kyritsi et al., 2018; Tobin, 1986). Concerns over energy use and scalding risk both favor the use of lower temperatures if possible. Therefore, there is a need to evaluate, and if possible reconcile, these studies in order to identify the lowest hot water temperature in plumbing systems that can control the growth of Legionella. In this study, our aim is to systematically review the evidence available on the association between hot water temperature and Legionella colonization and to conduct qualitative synthesis and meta-analysis to identify the required water temperature for controlling the risk of Legionella colonization.