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Preliminary Report on the Pathogenicity of Legionella Pneumophila for Freshwater and Soil Amoebae

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Preliminary Report on the Pathogenicity of Legionella Pneumophila for Freshwater and Soil Amoebae J Clin Pathol: first published as 10.1136/jcp.33.12.1179 on 1 December 1980. Downloaded from J Clin Pathol 1980;33:1179-1183 Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae TIMOTHY J ROWBOTHAM From the Leeds Regional Public Health Laboratory, Bridle Path, York Road, LSJ5 7TR, UK SUMMARY Legionella pneumophila, the causative organism of Legionnaires' disease, is pathogenic for free living, ubiquitous, freshwater, and soil amoebae of the genera Acanthamoeba and Naegleria. Some species support the growth of strains from serogroups 1 to 6, others only strains from certain serogroups. Initial studies with seeded material indicate that amoebal enrichment could be utilised for the isolation of legionellae from clinical specimens and natural habitats. It is suggested that a vacuole, or amoeba, full of legionellae, rather than free legionellae, could be the infective particle for man. Legionella pneumophila, the causative organism of is not a free living aquatic bacterium. Recently, a Legionnaires' disease, has been isolated from the relationship between L.pneumophila and a Fischerella water of coolingtowers,'-3evaporative condensers,2 4 sp. has been described. Growth of L.pneumophila ponds,5 a thermally polluted stream, the mud of that occurred only when the cyanobacteria were photo- stream,1 2 and various other aquatic habitats. synthesising.17 It will survive several months, or longer, in water for In man, L.pneumophila infects macrophages, in copyright. injection,6 and in distilled,7 8 tap,7 stream,9 and which large numbers of legionellae have been pond water.'0 However, laboratory media for the observed intracellularly.18-20 Extracellular legion- growthofL.pneumophilarequiresupplementationwith ellae appear to be closely associated with lysed L-cysteine and ferric iron, usually ferric pyrophos- macrophages.18 In-vitro studies with cynolmolgus phate. The main carbon sources for L.pneumophila monkey macrophages21 showed that L.pneumophila are L-amino acids. Arginine, cysteine, isoleucine, can grow in their cytoplasm and that, although rat leucine, methionine, threonine, valine, and phenyl- and mouse alveolar macrophages ingest only a alanine or tyrosine are required for growth. Most antibody-coated L.pneumophila,22 this is not http://jcp.bmj.com/ strains require serine, some also require proline. necessary prerequisite for phagocytosis by cynol- Serine and, to a lesser extent, threonine can be used molgus monkey macrophages.2' Intracellular as sole sources of carbon and energy." 12 Carbo- L.pneumophila in polymorphonuclear leucocytes hydrates" 13 and many organic acids are not appears to be rare.'8 23 Macrophages are amoeboid utilised, while some organic acids, for example, cells and, because of the similarity between macro- citric and oleic acid, are inhibitory." Growth on phages and amoebae, this study was initiated to solid media is initiated only within a narrow pH determine the interactions of L.pneumophila and range, around 6-9 (6.3-7-28).14'5 The optimum similar organisms with amoebae. Free living on September 28, 2021 by guest. Protected incubation conditions are 35°C in air +2-5% (v/v) amoebae of the genera Naegleria and Acanthamoeba C02; no growth occurs anaerobically. The temp- are ubiquitous in soil and water. The commonest erature range over which growth can occur is species, A.polyphaga, A.castellanii, and N.gruberi, approximately 251"-40'C. On first isolation, have been isolated from humidifiers and may be growth is usually very slow; only pin-point colonies present there in large numbers.24 are seen after three days. Growth of L.pneumophila on solid media is inhibited by many bacteria, for Methods example, certain members of the oral flora, a Bacillus species'6 and Pseudomonas aeruginosa, also CULTURE by a purified pyocin (unpublished data). These Ninety millimetre diameter plates of Stoianovitch's cultural characteristics indicate that L.pneumophila malt extract, yeast extract agar,25 prepared with Page's amoebal saline,25 pH 6-9, were flooded with a Received for publication 26 July 1980 turbid suspension of Klebsiella aerogenes (NCTC 1179 J Clin Pathol: first published as 10.1136/jcp.33.12.1179 on 1 December 1980. Downloaded from 1180 Rowbotham 7427) in amoebal saline, drained, and incubated firmed by immunofluorescence but not of those aerobically overnight at 350C. The agar was divided intracellularly, as antibody does not enter intact into two semicircular sections by the removal of a amoebae. diagonal 10 mm wide strip. To kill the klebsiellae, the open plates were exposed for 30 minutes to the Results and discussion UV light of a microbiological safety cabinet. One end of each semicircular lawn was inoculated with The Oxford-I29-31 strain of L.pneumophila isolated a suspension of amoebal trophozoites, and approx- from a patient in an Oxford renal transplant unit29 imately 15-20 mm away a line of L.pneumophila was chosen for special study because it was a recent was drawn with a wire across the semicircle so that isolate and thus less likely to be laboratory-adapted, the advancing amoebae would have to cross it. The and because similar strains had been isolated from wire was inoculated with legionellae from an the sieves of the transplant unit showers (JO'H enriched blood agar26 (with soluble starch 1-5 g/l, Tobin and RG Mitchell, personal communication). and L-serine 1-0 g/l) plate, incubated at 350C, in The slowest growing amoeba, Acanthamoeba air + 2-5 % v/v C02, for three to five days. On the castellanii, took about five days to reach the line of control side, UV-killed klebsiellae were used. legionellae. After two days in contact with the Amoebal cultures were incubated aerobically at line there was no advance of the amoebae beyond 30'C, the sump temperature of the type of the line. The amoebae in contact with the line were humidifiers from which L.pneumophila has been usually rounded up, smaller, and vacuolate; some isolated.27 were lysed. Heavily infected amoebae (Fig. 1) MICROSCOPY The amoebae were examined microscopically in situ on the agar surface with a x 40 12 mm working distance objective (Vickers Instruments, Haxby Road, York). Isolation of single cysts and amoebae was facilitated by the long working distance of this copyright. objective and the absence of image inversion and reversion. For higher magnifications, amoebae were suspended in one drop of amoebal saline on a *:~~~~~~~~~~~~~~~.....:: 22 x 64 mm cover slip. Small drops of glycerol were placed at each end, and a cavity slide was inverted over the cover slip. The mount was left s~~~~~~~~sR~ ~... ... ..I... in that position for at least 20 minutes to allow the Kfi 7I||I .:' the Fi. Acstlai troot inece wit the amoebae to extend and adhere to the cover slip; http://jcp.bmj.com/ slide was inverted for examination. After examina- tion of the live material the slide was removed, klbselae 1exrclua leinla arud h and 3 drops of hot (- 80C) 10% (v/v) formalin were added to the amoebal drop just before it dried. After 2 minutes the cover slip was immersed for 2 minutes in unheated 10% (v/v) formalin, rinsed vauoesameb.::~~~~~~~~~~~~~4Th leionellae in th vacuol.,es. in tap water, air dried, and stained by a modifi- amoeba.~~~~~~~~~~~~~~~~~~~~WN~_ on September 28, 2021 by guest. Protected cation of the Gimenez technique,28 in which the Fig. n A.castellanii trophozoite infected with the buffered carbol fuchsin was warmed to 500C, Oxford-l strain of L.pneumophila. Modified Cimenez filtered on to the cover slip, and left for 10 minutes. stain. L = endoplasmic vacuole containing legionellae; After thorough washing in tap water, the cover slip nw= nucleus; c contractile vacuole; kf= extracellular was stained with aqueous malachite green (8 g/l) for klebsiellae; f extracellular legionellae around the 5-10 seconds, washed in tap water, stained again amoeba. with the malachite green for 5-10 seconds, washed in tap water, and finally stained with aqueous occurred in the vicinity of the line. The infection methylene blue (40 mg/l) for 60-90 seconds, washed, was confined to vacuoles, often up to 10-15 and dried. With this technique klebsiellae (cocco- vacuoles/amoeba. The legionellae in the vacuoles bacilli) were blue to pale pink, rarely maroon, were non-motile. In some rare amoebae, the infection legionellae (bacilli) pink to maroon, amoebal was not confined, and these amoebae developed cytoplasm pale blue, and nucleus blue-grey. The into bags of non-motile legionellae. This latter type identity of the extracellular bacteria can be con- of infection was more common with the other J Clin Pathol: first published as 10.1136/jcp.33.12.1179 on 1 December 1980. Downloaded from L.pneumophila, an amoebal pathogen 1181 L.pneumophila strains and is similar to that seen in behind the line and between the line and the advanc- human18 and monkey2' macrophages. In prepara- ing edge of amoebal growth. No cysts or malformed tions of live material, some amoebae contained amoebae were seen at the advancing edge of amoebal numerous large vacuoles, but even heavily infected growth. In hanging drop preparations, the amoebae amoebae usually produced pseudopodia. On the usually appeared normal, but some rare amoebae had control side, the amoebae advanced beyond the a single large endoplasmic vacuole containing many line of dead klebsiellae; no legionellae could be rapidly motile bacilli. These infected amoebae were demonstrated in those amoebae. Small groups of still moving, and apparently feeding, explaining legionellae and single legionella in recently infected how infected amoebae and failed cysts could be amoebae could be demonstrated only by staining. found behind the inoculum line. Large vesicles Some amoebae were so heavily infected (Fig. 1) that presumably from ruptured or lysed amoebae were the infection could only be fatal. Infected amoebae rare, but some of these also contained rapidly were easily ruptured.
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