Evaluation of an immunomagnetic separation assay in combination with cultivation to improve Legionella pneumophila serogroup 1 recovery from environmental samples

Journal of Applied Microbiology

Volumn 110, Issue 4, 2011, Pages 952-961

  Allegra, S ^a   Girardot, F ^a   Grattard, F ^a   Berthelot, P ^a   Helbig, J H ^b   Pozzetto, B ^a   Riffard, S ^a  

^a UNIVERSITÉ JEAN MONNET   (France)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Culture; Environmental samples; Immunomagnetic separation; Legionella; Monoclonal antibody

Indexed keywords

ISO STANDARDS;

ASSOCIATED BACTERIA; CONFIDENCE LIMIT; CULTURE; ENVIRONMENTAL SAMPLE; IMMUNOMAGNETIC SEPARATION; LEGIONELLA PNEUMOPHILA; LEGIONELLAE; LIPOPOLYSACCHARIDES; SEROGROUPS; WATER SAMPLES;

MONOCLONAL ANTIBODIES;

COOLING WATER; GROUND WATER; HOT WATER; LIPOPOLYSACCHARIDE; MONOCLONAL ANTIBODY;

ANTIBODY; ASSAY; BACTERIUM; BIOFILM; CULTIVATION; DETECTION METHOD; FREQUENCY ANALYSIS; HETEROTROPHY; IMMUNE SYSTEM; LIPID; PERFORMANCE ASSESSMENT; POLYSACCHARIDE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATION; BIOFILM; CLINICAL EVALUATION; COLONY FORMING UNIT; COOLING TOWER; IMMUNOMAGNETIC SEPARATION; LEGIONELLA PNEUMOPHILA; NONHUMAN; PSEUDOMONAS AERUGINOSA; SPECIES CULTIVATION; WATER SAMPLING; CLASSIFICATION; EVALUATION STUDY; IMMUNOLOGY; ISOLATION AND PURIFICATION; MICROBIOLOGY; PROCEDURES; SEROTYPE;

LEGIONELLA; LEGIONELLA PNEUMOPHILA; LEGIONELLA PNEUMOPHILA SEROGROUP 1;

BIOFILMS; ENVIRONMENTAL MICROBIOLOGY; IMMUNOMAGNETIC SEPARATION; LEGIONELLA PNEUMOPHILA; SEROGROUP; WATER MICROBIOLOGY;

EID: 79954621594     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2011.04955.x     Document Type: Article

References (54)

1. Aurell, H., Catala, P., Farge, P., Wallet, F., Le Brun, M., Helbig, J.H., Jarraud, S. and Lebaron, P. (2004) Rapid detection and enumeration of Legionella pneumophila in hot water systems by Solid-Phase Cytometry. Appl Environ Microbiol 70, 1651-1657.
2. Bartie, C., Venter, S.N. and Nel, L.H. (2003) Identification methods for Legionella from environmental samples. Water Res 37, 1362-1370.
3. Behets, J., Declerck, P., Delaedt, Y., Creemers, B. and Ollevier, F. (2007) Development and evaluation of a Taqman duplex real-time PCR quantification method for reliable enumeration of Legionella pneumophila in water samples. J Microbiol Methods 68, 137-144.
4. Brichta-Harhay, D.M., Guerini, M.N., Arthur, T.M., Bosilevac, J.M., Kalchayanand, N., Shackelford, S.D., Wheeler, T.L. and Koohmaraie, M. (2008) Salmonella and Escherichia coli O157:H7 contamination on hides and carcasses of cull cattle presented for slaughter in the United States: an evaluation of prevalence and bacterial loads by immunomagnetic separation and direct plating methods. Appl Environ Microbiol 74, 6289-6297.
5. Buchbinder, S., Trebesius, K. and Heesemann, J. (2002) Evaluation of detection of Legionella spp. in water samples by fluorescence in situ hybridization, PCR amplification and bacterial culture. Int J Med Microbiol 292, 241-245.
6. Chang, B., Sugiyama, K., Taguri, T., Amemura-Maekawa, J., Kura, F. and Watanabe, H. (2009) Specific detection of viable Legionella cells by combined use of photoactivated ethidium monoazide and PCR/real-time PCR. Appl Environ Microbiol 75, 147-153.
7. DeCory, T.R., Durst, R.A., Zimmerman, S.J., Garringer, L.A., Paluca, G., DeCory, H.H. and Montagna, R.A. (2005) Development of an immunomagnetic bead-immunoliposome fluorescence assay for rapid detection of Escherichia coli O157:H7 in aqueous samples and comparison of the assay with a standard microbiological method. Appl Environ Microbiol 71, 1856-1864.
8. Deng, M.Q., Lam, K.M. and Cliver, D.O. (2000) Immunomagnetic separation of Cryptosporidium parvum oocysts using MACS MicroBeads and high gradient separation columns. J Microbiol Methods 40, 11-17.
9. Drinking-Water-Inspectorate (2000) Comparison of Methods for Drinking Water Bacteriology - Cultural Techniques. London, UK: Department of the Environment, Transport and the Regions.
10. Duan, H.L., Shen, Z.Q., Wang, X.W., Chao, F.H. and Li, J.W. (2005) Preparation of immunomagnetic iron-dextran nanoparticles and application in rapid isolation of E.coli O157:H7 from foods. World J Gastroenterol 11, 3660-3664.
11. Dusserre, E., Ginevra, C., Hallier-Soulier, S., Vandenesch, F., Festoc, G., Etienne, J., Jarraud, S. and Molmeret, M. (2008) A PCR-based method for monitoring Legionella pneumophila in water samples detects viable but noncultivable legionellae that can recover their cultivability. Appl Environ Microbiol 74, 4817-4824.
12. Edelstein, P.H. (1982) Comparative study of selective media for isolation of Legionella pneumophila from potable water. J Clin Microbiol 16, 697-699.
13. Enroth, H. and Engstrand, L. (1995) Immunomagnetic separation and PCR for detection of Helicobacter pylori in water and stool specimens. J Clin Microbiol 33, 2162-2165.
14. Favrin, S.J., Jassim, S.A. and Griffiths, M.W. (2001) Development and optimization of a novel immunomagnetic separation- bacteriophage assay for detection of Salmonella enterica serovar enteritidis in broth. Appl Environ Microbiol 67, 217-224.
15. Fuchslin, H.P., Kotzsch, S., Keserue, H.A. and Egli, T. (2010) Rapid and quantitative detection of Legionella pneumophila applying immunomagnetic separation and flow cytometry. Cytometry A 77, 264-274.
16. Ginevra, C., Barranger, C., Ros, A., Mory, O., Stephan, J.L., Freymuth, F., Joannes, M., Pozzetto, B. et al. (2005) Development and evaluation of Chlamylege, a new commercial test allowing simultaneous detection and identification of Legionella, Chlamydophila pneumoniae, and Mycoplasma pneumoniae in clinical respiratory specimens by multiplex PCR. J Clin Microbiol 43, 3247-3254.
17. Gottschalk, M., Lacouture, S. and Odierno, L. (1999) Immunomagnetic isolation of Streptococcus suis serotypes 2 and 1/2 from swine tonsils. J Clin Microbiol 37, 2877-2881.
18. Grattard, F., Berthelot, P., Reyrolle, M., Ros, A., Etienne, J. and Pozzetto, B. (1996) Molecular typing of nosocomial strains of Legionella pneumophila by arbitrarily primed PCR. J Clin Microbiol 34, 1595-1598.
19. Hallier-Soulier, S. and Guillot, E. (2003) An immunomagnetic separation-reverse transcription polymerase chain reaction (IMS-RT-PCR) test for sensitive and rapid detection of viable waterborne Cryptosporidium parvum. Environ Microbiol 5, 592-598.
20. Helbig, J.H., Ludwig, B., Luck, P.C., Groh, A., Witzleb, W. and Hacker, J. (1995) Monoclonal antibodies to Legionella Mip proteins recognize genus- and species-specific epitopes. Clin Diagn Lab Immunol 2, 160-165.
21. Helbig, J.H., Kurtz, J.B., Pastoris, M.C., Pelaz, C. and Luck, P.C. (1997) Antigenic lipopolysaccharide components of Legionella pneumophila recognized by monoclonal antibodies: possibilities and limitations for division of the species into serogroups. J Clin Microbiol 35, 2841-2845.
22. Hibi, K., Abe, A., Ohashi, E., Mitsubayashi, K., Ushio, H., Hayashi, T., Ren, H. and Endo, H. (2006) Combination of immunomagnetic separation with flow cytometry for detection of Listeria monocytogenes. Anal Chim Acta 573-574, 158-163.
23. Hibi, K., Ushio, H., Fukuda, H., Mitsubayashi, K., Hayashi, T., Ren, H. and Endo, H. (2008) Immunomagnetic separation using carbonyl iron powder and flow cytometry for rapid detection of Flavobacterium psychrophilum. Anal Bioanal Chem 391, 1147-1152.
24. Islam, D., Tzipori, S., Islam, M. and Lindberg, A.A. (1993) Rapid detection of Shigella dysenteriae and Shigella flexneri in faeces by an immunomagnetic assay with monoclonal antibodies. Eur J Clin Microbiol Infect Dis 12, 25-32.
25. ISO 11731. (1998) Water Quality-detection and Enumeration of Legionella. Geneva, Switzerland: International Standards Organisation (ISO).
26. ISO 17994. (2004) Water Quality. Criteria for Establishing Equivalence Between Microbiological Methods. Geneva, Switzerland: International Organization for Standardization (ISO).
27. Joly, J.R., McKinney, R.M., Tobin, J.O., Bibb, W.F., Watkins, I.D. and Ramsay, D. (1986) Development of a standardized subgrouping scheme for Legionella pneumophila serogroup 1 using monoclonal antibodies. J Clin Microbiol 23, 768-771.
28. Joly, P., Falconnet, P.A., Andre, J., Weill, N., Reyrolle, M., Vandenesch, F., Maurin, M., Etienne, J. et al. (2006) Quantitative real-time Legionella PCR for environmental water samples: data interpretation. Appl Environ Microbiol 72, 2801-2808.
29. Karpova, T.I., Dronina Iu, E., Tartakovskii, I.S., Romanova Iu, M. and Gintsburg, A.L. (2008) Legionella natural biofilms and their role in epidemiology of the infection: methods of study and modelling. Zh Mikrobiol Epidemiol Immunobiol, 1, 3-7.
30. Kimura, S., Tateda, K., Ishii, Y., Horikawa, M., Miyairi, S., Gotoh, N., Ishiguro, M. and Yamaguchi, K. (2009) Pseudomonas aeruginosa Las quorum sensing autoinducer suppresses growth and biofilm production in Legionella species. Microbiology 155, 1934-1939.
31. Lee, J. and Deininger, R.A. (2004) Detection of E. coli in beach water within 1hour using immunomagnetic separation and ATP bioluminescence. Luminescence 19, 31-36.
32. Lehtola, M.J., Torvinen, E., Kusnetsov, J., Pitkanen, T., Maunula, L., von Bonsdorff, C.H., Martikainen, P.J., Wilks, S.A. et al. (2007) Survival of Mycobacterium avium, Legionella pneumophila, Escherichia coli, and caliciviruses in drinking water-associated biofilms grown under high-shear turbulent flow. Appl Environ Microbiol 73, 2854-2859.
33. Lemarchand, K., Parthuisot, N., Catala, P. and Lebaron, P. (2001) Comparative assessment of epifluorescence microscopy, flow cytometry and solid-phase cytometry used in the enumeration of specific bacteria in water. Aquat Microb Ecol 25, 301-309.
34. Leoni, E. and Legnani, P.P. (2001) Comparison of selective procedures for isolation and enumeration of Legionella species from hot water systems. J Appl Microbiol 90, 27-33.
35. Li, Z., Bai, G.H., von Reyn, C.F., Marino, P., Brennan, M.J., Gine, N. and Morris, S.L. (1996) Rapid detection of Mycobacterium avium in stool samples from AIDS patients by immunomagnetic PCR. J Clin Microbiol 34, 1903-1907.
36. Luck, P.C., Igel, L., Helbig, J.H., Kuhlisch, E. and Jatzwauk, L. (2004) Comparison of commercially available media for the recovery of Legionella species. Int J Hyg Environ Health 207, 589-593.
37. NF T90-431. (2003) Water Quality-detection and Enumeration of Legionella spp and Legionella pneumophila. Method by Direct Culture Inoculation and After Concentration by Membrane Filtration or Centrifugation. Paris, France: Association Française de Normalisation (AFNOR).
38. NF T90-471. (2010) Water quality-detection and Enumeration of Legionella spp and Legionella pneumophila by Concentration and Real-time Polymerase Chain Reaction (RT-PCR). Paris, France: Association Française de Normalisation (AFNOR).
39. Ochiai, Y., Takada, C. and Hosaka, M. (2005) Detection and discrimination of Cryptosporidium parvum and C. hominis in water samples by immunomagnetic separation-PCR. Appl Environ Microbiol 71, 898-903.
40. Olsvik, O., Popovic, T., Skjerve, E., Cudjoe, K.S., Hornes, E., Ugelstad, J. and Uhlen, M. (1994) Magnetic separation techniques in diagnostic microbiology. Clin Microbiol Rev 7, 43-54.
41. Pitkänen, T., Paakkari, P., Miettinen, I.T., Heinonen-Tanski, H., Paulin, L. and Hänninen, M.L. (2007) Comparison of media for enumeration of coliform bacteria and Escherichia coli in non-disinfected water. J Microbiol Methods 68, 522-529.
42. Riffard, S., Douglass, S., Brooks, T., Springthorpe, S., Filion, L.G. and Sattar, S.A. (2001) Occurrence of Legionella in groundwater: an ecological study. Water Sci Technol 43, 99-102.
43. Ripabelli, G., Sammarco, M.L. and Grasso, G.M. (1999) Evaluation of immunomagnetic separation and plating media for recovery of Salmonella from meat. J Food Prot 62, 198-201.
44. Robinson, G., Watkins, J. and Chalmers, R.M. (2008) Evaluation of a modified semi-automated immunomagnetic separation technique for the detection of Cryptosporidium oocysts in human faeces. J Microbiol Methods 75, 139-141.
45. Rochelle, P.A., De Leon, R., Johnson, A., Stewart, M.H. and Wolfe, R.L. (1999) Evaluation of immunomagnetic separation for recovery of infectious Cryptosporidium parvum oocysts from environmental samples. Appl Environ Microbiol 65, 841-845.
46. Sartory, D.P. (2005) Validation, verification and comparison: adopting new methods in water microbiology. Water SA 31, 393-396.
47. Seo, K.H., Brackett, R.E. and Frank, J.F. (1998) Rapid detection of Escherichia coli O157:H7 using immuno-magnetic flow cytometry in ground beef, apple juice, and milk. Int J Food Microbiol 44, 115-123.
48. Sethi, S., Gore, M.T. and Sethi, K.K. (2007) Increased sensitivity of a direct fluorescent antibody test for Legionella pneumophila in bronchoalveolar lavage samples by immunomagnetic separation based on BioMags. J Microbiol Methods 70, 328-335.
49. Skjerve, E. and Olsvik, O. (1991) Immunomagnetic separation of Salmonella from foods. Int J Food Microbiol 14, 11-17.
50. Sorel, N., Guillot, E., Thellier, M., Accoceberry, I., Datry, A., Mesnard-Rouiller, L. and Miegeville, M. (2003) Development of an immunomagnetic separation-polymerase chain reaction (IMS-PCR) assay specific for Enterocytozoon bieneusi in water samples. J Appl Microbiol 94, 273-279.
51. Tomoyasu, T. (1998) Improvement of the immunomagnetic separation method selective for Escherichia coli O157 strains. Appl Environ Microbiol 64, 376-382.
52. Wang, X. and Slavik, M.F. (1999) Rapid detection of Salmonella in chicken washes by immunomagnetic separation and flow cytometry. J Food Prot 62, 717-723.
53. Wilks, S.A. and Keevil, C.W. (2006) Targeting species-specific low-affinity 16S rRNA binding sites by using peptide nucleic acids for detection of Legionellae in biofilms. Appl Environ Microbiol 72, 5453-5462.
54. Yanez, M.A., Carrasco-Serrano, C., Barbera, V.M. and Catalan, V. (2005) Quantitative detection of Legionella pneumophila in water samples by immunomagnetic purification and real-time PCR amplification of the dotA gene. Appl Environ Microbiol 71, 3433-3441.