Elsevier

Water Research

Volume 46, Issue 4, 15 March 2012, Pages 921-933
Water Research

Review
Legionellae in engineered systems and use of quantitative microbial risk assessment to predict exposure

https://doi.org/10.1016/j.watres.2011.12.022Get rights and content

Abstract

While it is well-established that Legionella are able to colonize engineered water systems, the number of interacting factors contributing to their occurrence, proliferation, and persistence are unclear. This review summarizes current methods used to detect and quantify legionellae as well as the current knowledge of engineered water system characteristics that both favour and promote legionellae growth. Furthermore, the use of quantitative microbial risk assessment (QMRA) models to predict potentially critical human exposures to legionellae are also discussed. Understanding the conditions favouring Legionella occurrence in engineered systems and their overall ecology (growth in these systems/biofilms, biotic interactions and release) will aid in developing new treatment technologies and/or systems that minimize or eliminate human exposure to potentially pathogenic legionellae.

Highlights

► We review current legionellae detection and quantification methods. ► We discuss conditions favouring Legionellae occurrence in engineered systems. ► Quantitative microbial risk assessment is a tool to predict legionella exposure risk. ► We emphasize the need and rationale to better understand legionellae ecology.

Introduction

Legionellosis associated with engineered water systems (e.g. piped drinking water, cooling towers, fountains and humidifiers) continue to cause major outbreaks (Craun et al., 2010, Diederen, 2008, Fields et al., 2002, Sonder et al., 2008, Steinert et al., 2002) and may also contribute to a significant amount of community acquired pneumonia (CAP) cases (Cilloniz et al., 2011, Craun et al., 2010, Song et al., 2011). In assessing the occurrence of legionellae in engineered water systems, most standards describe culture-based methods (International Organization for Standardization, 1998). However, there is mounting evidence that viable or active but non-culturable (ABNC) Legionella spp. are present at densities 0.6 to 2.0 logs higher than colony forming units (CFU), and some fraction of these ABNC cells may still be infectious to humans (Borella et al., 2005a, Steinert et al., 1997). Furthermore, given human disease is known to result from 25 of the 54 species of Legionella currently described (Bartram et al., 2007, Yang et al., 2011) and that the panoply of virulence factors acquired by various legionellae occurs in its biofilm niche, it is unclear what the diversity of potential opportunistic pathogenic legionellae is (Gomez-Valero et al., 2009).

Given the uncertainties associated with standard CFU counts of legionellae on selective media or qPCR estimates of total legionellae, control has focused on eliminating conditions known to increase the presence of Legionella in engineered water systems (WHO, 2011). Despite uncertainties in Legionella ecology within engineered water systems (Steinert et al., 2002), there are several conditions known to favour growth and aerosol dissemination that are the focus of this review. Also discussed is the poor control efficacy for legionellae by low disinfectant residuals or various heat treatments for premise plumbing, given that persistent, active Legionella reservoirs are known to remain associated with amoebae/cysts in biofilms (Lau and Ashbolt, 2009, Storey et al., 2004b). Hence foremost in legionellae control is the reduction of warm-water and stagnation zones in drinking water systems (Hoebe and Kool, 2000) and use of residual biocide/cleaning to reduce biofilm build up within cooling towers, whirlpools, fountains and humidifiers (Bartram et al., 2007).

Section snippets

Detection of environmental Legionella spp

Culture methods are traditionally used for detecting and quantifying legionellae, but they generally underestimate cell densities by 10–60 % (Lee et al., 2002). Moreover, culture techniques have been optimized for Legionella pneumophila and may not be suitable for all Legionella species, including Legionella-like amoebal pathogens (LLAPs). Low culture recovery may also be due to the processes involved in the preparation of samples for culture (concentration, acid/heat pretreatment, presence of

Diversity of Legionella in natural and engineered water systems

Legionellae have been reported to occur in freshwater environments and within engineered water systems at temperatures ranging from 0 to 60 °C (Carvalho et al., 2008, Martinelli et al., 2000) with the optimum growth temperature between 25 and 42 °C (Fields et al., 2002). Fig. 1 illustrates the various systems - natural, engineered and human impacted, where Legionella spp. have been described (Carvalho et al., 2007, Parthuisot et al., 2010, Wullings and van der Kooij, 2006) (values in Fig. 1

Key factors contributing to Legionella growth, persistence and risk

Many studies have statistically correlated water quality parameters such as temperature (20–50 °C), stagnation of piped water, nutrient/sediment content and type, and quantity of disinfectants in engineered systems to legionellae incidence and growth (summarized in Table 2). Ultimately, a better understanding of these risk factors and Legionella ecology will lead to the development of control strategies that should minimize human exposure to potentially pathogenic Legionella spp. in aerosols.

QMRA development

Quantitative Microbial Risk Assessment (QMRA) utilizes estimates of pathogen density and infectivity information to assess pathogen risk; for example, the risk of infection from inhalation of Legionella derived from various engineered water systems. The QMRA process involves: (i) hazard identification and characterization, (ii) exposure assessment, (iii) dose–response assessment, and (iv) risk characterization (US-EPA, 2007). These assessments aim to understand how the growth of Legionella,

Concluding remarks

This review addresses a consolidation of knowledge about engineered water systems that correlate with Legionella occurrence, proliferation and pathogenicity, and introduces the use of QMRA to assess human health risk from legionellae exposure. However, information regarding Legionella ecology within biofilms that shed light on their infectivity and proliferation is limited. This lack of understanding could be compounding the ineffectiveness of legionellae control efforts. In other words, how

Acknowledgements

The authors would like to thank Dr. Jay Garland and the two anonymous reviewers for their critical and constructive review of this manuscript. The United States Environmental Protection Agency through it Office of Research and Development reviewed and approved this work for publication.

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