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18167638.Pdf REVIEW ARTICLE Amoebal pathogens as emerging causal agents of pneumonia Fred´ eric´ Lamoth1 & Gilbert Greub1,2 1Infectious Diseases Service, University of Lausanne, Lausanne, Switzerland; and 2Center for Research on Intracellular Bacteria, Institute of Microbiology, University Hospital Center and University of Lausanne, Lausanne, Switzerland Correspondence: Gilbert Greub, Center for Abstract Research on Intracellular Bacteria, Institute of Microbiology, University Hospital Center and Despite using modern microbiological diagnostic approaches, the aetiological University of Lausanne, Rue du Bugnon 46, agents of pneumonia remain unidentified in about 50% of cases. Some bacteria 1011 Lausanne, Switzerland. Tel.: 141 21 that grow poorly or not at all in axenic media used in routine clinical bacteriology 31449 79; fax: 141 21 31440 60; e-mail: laboratory but which can develop inside amoebae may be the agents of these lower [email protected] respiratory tract infections (RTIs) of unexplained aetiology. Such amoebae- resisting bacteria, which coevolved with amoebae to resist their microbicidal Received 24 September 2009; revised 30 machinery, may have developed virulence traits that help them survive within November 2009; accepted 2 December 2009. human macrophages, i.e. the first line of innate immune defence in the lung. We Final version published online 22 January 2010. review here the current evidence for the emerging pathogenic role of various DOI:10.1111/j.1574-6976.2009.00207.x amoebae-resisting microorganisms as agents of RTIs in humans. Specifically, we discuss the emerging pathogenic roles of Legionella-like amoebal pathogens, novel Editor: Colin Berry Chlamydiae (Parachlamydia acanthamoebae, Simkania negevensis), waterborne mycobacteria and Bradyrhizobiaceae (Bosea and Afipia spp.). Keywords free-living amoebae; amoebae-resisting bacteria; Legionella; Chlamydia-like bacteria; mycobacteria; pneumonia. some extent, agents of pneumonia have been identified in Introduction the context of outbreaks or case series occurring in a Despite advances in antibiotic therapy, pneumonia remains particular setting. For instance, psittacosis (parrot fever) one of the leading infectious causes of death in developed was described for the first time in seven individuals exposed countries and a major cause of morbidity, especially in the to pet birds in Switzerland in the 19th century (Ritter, 1880). elderly population and among patients with chronic under- More recently, the epidemics of severe pneumonia affecting lying diseases (Mandell et al., 2007). Although a broad war veterans in a hotel in Philadelphia in 1976 led to the spectrum of microbial pathogens have been recognized as discovery of the fastidious gram-negative rod Legionella causal agents of respiratory tract infections (RTIs), the pneumophila as a causal agent of respiratory diseases (Fraser offending microorganism remains unknown in about half et al., 1977; McDade et al., 1977). In this latter situation, of the cases of community-acquired pneumonia (CAP) water was found to be the source of contamination. Rowbo- (Bochud et al., 2001; Echols et al., 2008), and three quarters tham (1980, 1983) then demonstrated that L. pneumophila of the cases of nosocomial pneumonia (Costa et al., 2001). may multiply within free-living amoebae and hypothesized Microorganisms causing pneumonia may be acquired that these protists may represent a reservoir for these from respiratory droplets through human-to-human con- intracellular bacteria. tact or from aerosolized particles from an animal or Free-living amoebae live in water, soil and at the water–air environmental reservoir. The epidemiology of RTI thus interface. As they generally use bacteria as their main strongly depends on the interactions between humans and nutritional source, they are especially present in large their ecosystem and evolves according to environmental quantities in sediments and biofilms (Rodriguez-Zaragoza, MICROBIOLOGY REVIEWS MICROBIOLOGY changes due to human activities, climatic or ecological 1994). Thus, humans have been increasingly exposed to perturbations. Pandemics of influenza or the emergence of amoebae and to their related bacterial pathogens with the new respiratory diseases such as severe acute respiratory progressive development of various modern man-made syndrome are dramatic illustrations of these phenomena. To water systems such as water-treatment plants, cooling c 2010 Federation of European Microbiological Societies FEMS Microbiol Rev 34 (2010) 260–280 Published by Blackwell Publishing Ltd. All rights reserved Amoebal pathogens as causal agents of pneumonia 261 towers, air conditioners, humidifiers, spas and swimming amoebal microorganisms. Both approaches have been suc- pools (Rodriguez-Zaragoza, 1994; Greub & Raoult, 2004; cessfully used in recent years to uncover a variety of Pagnier et al., 2009a). Apart from L. pneumophila, which has amoebae-resisting microorganisms from both environmen- mainly been recognized due to the dramatic importance of tal and clinical samples (Adekambi et al., 2004; Greub et al., the Philadelphia outbreak, many other bacteria that resist 2004b; Thomas et al., 2006, 2008; Loret et al., 2008; Corsaro the phagocytic amoebae may also use these protists as et al., 2009; Pagnier et al., 2009b). widespread reservoirs and may have acquired virulence traits promoting their resistance to macrophages. Interest- Understanding the pathogenic role of ingly, some of these amoebae-resisting bacteria have also amoebae-resisting bacteria: a been discovered during outbreaks of RTI (Herwaldt et al., 1984; Birtles et al., 1997). Indeed, given their intracellular comprehensive model approach lifestyle, they either do not grow or only poorly grow in The availability of a bacterial strain growing in amoebae conventional axenic media. It is important that the micro- allows its pathogenic potential to be tested, for instance as biology community be well aware of these new emerging an agent of pneumonia, using the comprehensive approach human agents of pneumonia and develop new diagnostic that has been applied to P. acanthamoebae (Greub, 2009). tools for their identification. Amoebal coculture and amoe- This global strategy includes (1) testing the permissiveness bal enrichment coupled with detection of potential intra- of lung fibroblasts, pneumocytes and alveolar macrophages amoebal bacteria have been demonstrated to be largely to the new bacterial species; (2) developing diagnostic tools successful in identifying a large biodiversity of new patho- (serology, antigen-detection assays, PCR and immunohisto- gens from patients (Greub et al., 2004b; Thomas et al., 2006; chemistry) to study patients with and without lower RTIs; Corsaro et al., 2009; Pagnier et al., 2009a, b). and (3) investigating the pathogenic role of some selected In this review, we intend to present the current evidence species in an animal model of pneumonia. For species that of the role of various amoebae-resisting bacteria as agents of emerge as new pathogens or exhibit very peculiar interesting RTI in humans. More specifically, we will discuss the likely biological phenotypes, the availability of a given strain also role of Legionella-like amoebal pathogens (LLAPs), novel allows better understanding of the biology of the species Chlamydiae (Parachlamydia acanthamoebae, Simkania nege- involved, using functional genomics, proteomics and cell vensis), waterborne mycobacteria and Bradyrhizobiaceae biology. (Bosea and Afipia spp.). Amoebal pathogens as causal agents of Diagnostic tools for the identification of pneumonia: clinical evidence amoebae-resisting bacteria Legionella species For a better characterization of the microbial biodiversity, various molecular approaches are available, including a Legionella pneumophila coupled cloning and sequencing approach, and metage- nomics using new pyrosequencing techniques such as the The potential role of water systems as a reservoir of human 454 and Solexa/Illumina technologies. However, such se- respiratory diseases was recognized for the first time when quence-based ecological studies do not provide the strains L. pneumophila was identified as the causal agent of an for subsequent studies, and consequently culture-based outbreak of pneumonia in Philadelphia in 1976 (Fraser ecological studies are of equal if not greater importance. et al., 1977; McDade et al., 1977). This bacterium is wide- However, most culture-based studies are biased towards spread in our aquatic environment including man-made bacteria able to grow efficiently on different axenic media, water systems and is one of the first examples of amoebae- broths and/or agar plates, and approaches that selectively resisting bacteria that has been described (Rowbotham, 1980, amplify amoebae-resisting bacteria may be useful. Two main 1983). It is estimated to account for 2–7% of all cases of CAP approaches, amoebal coculture and amoebal enrichment, affecting both immunocompromised and immunocompe- have been applied so far to recover amoebae-resisting tent hosts (Doebbeling & Wenzel, 1987; Marrie et al., 1989; bacteria in culture (Fig. 1). Amoebal coculture is a cell Fang et al., 1990a; Woodhead, 2002). Nosocomial outbreaks culture method in which axenic amoebae are used as a host of Legionnaires’ disease are also frequently reported and may cell culture, whereas amoebal enrichment uses an enteric result from bronchoaspiration of contaminated potable bacterium such as Escherichia coli as a food source for water rather than inhalation of
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