Fluorescence in situ Hybridization method using Peptide Nucleic Acid probes for rapid detection of Lactobacillus and Gardnerella spp.

BMC Microbiology

Volumn 13, Issue 1, 2013, Pages

  Machado, António ^a   Almeida, Carina ^a,b   Salgueiro, Débora ^a   Henriques, Ana ^a   Vaneechoutte, Mario ^c   Haesebrouck, Freddy ^d   Vieira, Maria João ^a   Rodrigues, Ligia ^a   Azevedo, Nuno Filipe ^b   Cerca, Nuno ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c GHENT UNIVERSITY   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

Bacterial vaginosis; Fluorescence in situ Hybridization (FISH); Gardnerella vaginalis; Lactobacillus spp.; Peptide Nucleic Acid Probe (PNA probe)

Indexed keywords

PEPTIDE NUCLEIC ACID;

ARTICLE; BACTERIAL STRAIN; BACTERIUM DETECTION; CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; GARDNERELLA INFECTION; GARDNERELLA VAGINALIS; HELA CELL; IN VITRO STUDY; LACTOBACILLUS; MOLECULAR PROBE; NONHUMAN; SENSITIVITY AND SPECIFICITY; TAXONOMY; VAGINA FLORA;

BACTERIOLOGICAL TECHNIQUES; FEMALE; GARDNERELLA VAGINALIS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; LACTOBACILLUS; OLIGONUCLEOTIDE PROBES; PEPTIDE NUCLEIC ACIDS; SENSITIVITY AND SPECIFICITY; VAGINOSIS, BACTERIAL;

BACTERIA (MICROORGANISMS); GARDNERELLA; GARDNERELLA VAGINALIS; LACTOBACILLUS;

EID: 84876910736     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-13-82     Document Type: Article

References (60)

1. Bacterial vaginosis. Spiegel CA, Clin Microbiol Rev 1991 4 485 502 1747864
2. The etiology of bacterial vaginosis. Turovskiy Y, Noll KS, Chikindas ML, J Appl Microbiol 2011 110 1105 1128 10.1111/j.1365-2672.2011.04977.x 21332897
3. Dynamics of vaginal bacterial communities in women developing bacterial vaginosis, candidiasis, or no infection, analyzed by PCR-denaturing gradient gel electrophoresis and real-time PCR. Vitali B, Pugliese C, Biagi E, Candela M, Turroni S, Bellen G, Donders GG, Brigidi P, Appl Environ Microbiol 2007 73 5731 5741 10.1128/AEM.01251-07 17644631
4. Diversity of human vaginal bacterial communities and associations with clinically defined bacterial vaginosis. Oakley BB, Fiedler TL, Marrazzo JM, Fredricks DN, Appl Environ Microbiol 2008 74 4898 4909 10.1128/AEM.02884-07 18487399
5. Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. Ling Z, Kong J, Liu F, Zhu H, Chen X, Wang Y, Li L, Nelson KE, Xia Y, Xiang C, BMC Genomics 2010 11 488 503 10.1186/1471-2164-11-488 20819230
6. Molecular identification of bacteria associated with bacterial vaginosis. Fredricks DN, Fiedler TL, Marrazzo JM, N Engl J Med 2005 353 1899 1911 10.1056/NEJMoa043802 16267321
7. Quantitative determination by real-time PCR of four vaginal Lactobacillus species, Gardnerella vaginalis and Atopobium vaginae indicates an inverse relationship between L. gasseri and L. iners. De Backer E, Verhelst R, Verstraelen H, Alqumber MA, Burton JP, Tagg JR, Temmerman M, Vannechoutte M, BMC Microbiol 2007 7 115 10.1186/1471-2180-7-115 18093311
8. New concepts in the etiology of bacterial vaginosis. Schwebke JR, Curr Infect Dis Rep 2009 11 143 147 10.1007/s11908-009-0021-7 19239805
9. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of Gram stain interpretation. Nugent R, Krohn M, Hillier S, J Clin Microbiol 1991 29 297 301 1706728
10. Adherent biofilms in bacterial vaginosis. Swidsinski A, Mendling W, Loening-Baucke V, Ladhoff A, Swidsinski S, Hale LP, Lochs H, Obstet Gynecol 2005 106 1013 1023 10.1097/01.AOG.0000183594.45524.d2 16260520
11. Relationship between hydrogen peroxide-producing strains of lactobacilli and vaginosis-associated bacterial species in pregnant women. Rosenstein IJ, Fontaine EA, Morgan DJ, Sheehan M, Lamont RF, Taylor-Robinson D, Eur J Clin Microbiol Infect Dis 1997 16 517 522 10.1007/BF01708235 9272387
12. Effect of biofilm phenotype on resistance of Gardnerella vaginalis to hydrogen peroxide and lactic acid. Patterson JL, Girerd PH, Karjane NW, Jefferson KK, Am J Obstet Gynecol 2007 197 170 e1-7 17689638
13. Analysis of adherence, biofilm formation and cytotoxicity suggests a greater virulence potential of Gardnerella vaginalis relative to other bacterial-vaginosis-associated anaerobes. Patterson JL, Stull-Lane A, Girerd PH, Jefferson KK, Microbiol 2010 156 392 399 10.1099/mic.0.034280-0
14. A review of fluorescence in situ hybridization (FISH): current status and future prospects. Nath J, Johnson KL, Biotech Histochem 2000 75 54 78 10.3109/10520290009064150 10941509
15. Recent advances in molecular techniques to study microbial communities in food-associated matrices and processes. Justé A, Thommad B, Lievens B, Food Microbiol 2008 25 745 761 10.1016/j.fm.2008.04.009 18620966
16. PNA and LNA throw light on DNA. Demidov VV, Trends Biotechnol 2003 21 4 7 10.1016/S0167-7799(02)00008-2 12480343
17. Rapid and specific detection of PCR products using light-up probes. Isacsson J, Cao H, Nordgren S, Svanvik N, Westman G, Kubista M, Sjöback R, Sehlstedt U, Mol Cell Probes 2000 14 321 328 10.1006/mcpr.2000.0321 11040096
18. Fluorescence in situ hybridization with peptide nucleic acid probes for rapid identification of Candida albicans directly from blood culture bottles. Rigby S, Procop GW, Haase G, Wilson D, Hall G, Kurtzman C, Oliveira K, Von Oy S, Hyldig-Nielsen JJ, Coull J, Stender H, J Clin Microbiol 2002 40 2182 2186 10.1128/JCM.40.6.2182-2186.2002 12037084
19. PNA for rapid microbiology. Stender H, Fiandaca M, Hyldig-Nielsen JJ, Coull J, J Microbiol Methods 2002 48 1 17 10.1016/S0167-7012(01)00340-2 11733079
20. Rapid identification of Staphylococcus aureus directly from blood cultures by fluorescence in situ hybridization with peptide nucleic acid probes. Oliveira K, Procop GW, Wilson D, Coull J, Stender H, J Clin Microbiol 2002 40 247 251 10.1128/JCM.40.1.247-251.2002 11773123
21. Multicenter evaluation of a Candida albicans peptide nucleic acid fluorescent in situ hybridization probe for characterization of yeast isolates from blood cultures. Wilson DA, Joyce MJ, Hall LS, Reller LB, Roberts GD, Hall GS, Alexander BD, Procop GW, J Clin Microbiol 2005 43 2909 2912 10.1128/JCM.43.6.2909-2912.2005 15956416
22. Evaluation of peptide nucleic acid-fluorescence in situ hybridization for identification of clinically relevant mycobacteria in clinical specimens and tissue sections. Lefmann M, Schweickert B, Buchholz P, Göbel B, Ulrichs T, Seiler P, Theegarten D, Moter A, J Clin Microbiol 2006 44 3760 3767 10.1128/JCM.01435-06 17021106
23. Utility of peptide nucleic acid fluorescence in situ hybridization for rapid detection of Acinetobacter spp. and Pseudomonas aeruginosa. Peleg AY, Tilahun Y, Fiandaca MJ, D'Agata EMC, Venkataraman L, Moellering RC, Eliopoulos GM, J Clin Microbiol 2009 47 830 832 10.1128/JCM.01724-08 19116347
24. PRIMROSE: a computer program for generating and estimating the phylogenetic range of 16S rRNA oligonucleotide probes and primers in conjunction with the RDP-II database. Ashelford K, Weightman A, Fry J, Nucleic Acids Res 2002 30 3481 3489 10.1093/nar/gkf450 12140334
25. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Cole J, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM, Nucleic Acids Res 2009 37 141 D145 10.1093/nar/gkn879 19004872
26. Fluorescence In Situ Hybridization Method Using a Peptide Nucleic Acid Probe for Identification of Lactobacillus spp. in Milk Samples. Machado A, Almeida C, Carvalho A, Boyen F, Haesebrouck F, Rodrigues L, Cerca N, Azevedo NF, Int J of Food Microbiol 2013 162 64 70 10.1016/j.ijfoodmicro.2012.09.024
27. A fluorescence in situ hybridization method using a peptide nucleic acid probe for the identification of Salmonella spp. in a broad spectrum of samples. Almeida C, Azevedo NF, Fernandes R, Keevil C, Vieira MJ, Appl Environ Microbiol 2010 76 4476 4485 10.1128/AEM.01678-09 20453122
28. A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridization. Harmsen H, Elfferich P, Schut F, Welling G, Microb Ecol Health D 1999 11 3 12 10.1080/089106099435862
29. Specific oligonucleotide probes for in situ detection of a major group of gram-positive bacteria with low DNA G + C content. Meier H, Amann R, Ludwig W, Schleifer K, Syst Appl Microbiol 1999 22 186 196 10.1016/S0723-2020(99)80065-4 10390869
30. Oral biofilm architecture on natural teeth. Zijnge V, van Leeuwen MB, Degener JE, Abbas F, Thurnheer T, Gmur R, Harmsen HJ, PLoS ONE 2010 5 9321 10.1371/journal.pone.0009321 20195365
31. Digoxigenin-labelled peptide nucleic acid to detect lactobacilli PCR amplicons immobilized on membranes from denaturing gradient gel electrophoresis. Burton J, McCormick J, Cadieux P, Reid G, Lett Appl Microbiol 2003 36 145 149 10.1046/j.1472-765X.2003.01281.x 12581372
32. Changes in vaginal bacterial concentrations with intravaginal metronidazole therapy for bacterial vaginosis as assessed by quantitative PCR. Fredricks DN, Fiedler TL, Thomas KK, Mitchell CM, Marrazzo JM, J Clin Microbiol 2009 47 721 726 10.1128/JCM.01384-08 19144794
33. High levels of Gardnerella vaginalis detected with an oligonucleotide probe combined with elevated pH as a diagnostic indicator of bacterial vaginosis. Sheiness D, Dix K, Watanabe S, Hillier SL, J Clin Microbiol 1992 30 642 648 1372621
34. FISH analysis of Lactobacillus biofilms in the gastrointestinal tract of different hosts. Lebeer S, Verhoeven T, Claes I, De Hertogh G, Vermeire S, Buyse J, Van Immerseel F, Vanderleyden J, De Keersmaecker SC, Lett Appl Microbiol 2011 52 220 226 10.1111/j.1472-765X.2010.02994.x 21204880
35. Investigation of chicken intestinal bacterial communities by 16S rRNA targeted fluorescence in situ hybridization. Olsen K, Henriksen M, Bisgaard M, Nielsen O, Christensen H, Antonie van Leeuwenhoek 2008 94 423 437 10.1007/s10482-008-9260-0 18568414
36. Phylogenetic group- and species-specific oligonucleotide probes for single-cell detection of lactic acid bacteria in oral biofilms. Quevedo B, Giertsen E, Zijnge V, Lüthi-Schaller H, Guggenheim B, Thurnheer T, Gmur R, BMC Microbiol 2011 11 14 10.1186/1471-2180-11-14 21247450
37. Development and application of a novel peptide nucleic acid Probe for the specific detection of Chronobacter genomospecies (Enterobacter sakazakii) in powdered infant formula. Almeida C, Azevedo NF, Iversen C, Fanning S, Keevil C, Vieira MJ, Appl Environ Microbiol 2009 75 2925 2930 10.1128/AEM.02470-08 19270117
38. Quantitative analysis of diverse Lactobacillus species present in advanced dental caries. Byun R, Nadkarni MA, Chhour KL, Martin FE, Jacques NA, Hunter N, J Clin Microbiol 2004 42 3128 3136 10.1128/JCM.42.7.3128-3136.2004 15243071
39. Simultaneous identification of 14 genital microorganisms in urine by use of a multiplex PCR-based reverse line blot assay. McKechnie ML, Hillman R, Couldwell D, Kong F, Freedman E, Wang H, Gilbert GL, J Clin Microbiol 2009 47 1871 1877 10.1128/JCM.00120-09 19357202
40. Quantitative PCR assessments of bacterial species in women with and without bacterial vaginosis. Zozaya-Hinchliffe M, Lillis R, Martin DH, Ferris MJ, J Clin Microbiol 2010 48 1812 1819 10.1128/JCM.00851-09 20305015
41. Lactobacillus strains isolated from the vaginal microbiota of healthy women inhibit Prevotella bivia and Gardnerella vaginalis in coculture and cell culture. Atassi F, Brassart D, Grob P, Graf F, Servin AL, FEMS Immunol Med Microbiol 2006 48 424 432 10.1111/j.1574-695X.2006.00162.x 17059467
42. Characterization of the adherence properties of human Lactobacilli strains to be used as vaginal probiotics. Martín R, Sánchez B, Suárez JE, Urdaci MC, FEMS Microbiol Lett 2012 328 166 173 10.1111/j.1574-6968.2011.02495.x 22224921
43. Lactobacillus fermentum attenuates the proinflammatory effect of Yersinia enterocolitica on human epithelial cells. Frick JS, Schenk K, Quitadamo M, Kahl F, Köberle M, Bohn E, Aepfelbacher M, Autenrieth IB, Inflamm Bowel Dis 2007 13 83 90 10.1002/ibd.20009 17206643
44. Usefulness of epifluorescence for quantitative analysis of lactobacilli in probiotic feed. Bernardeau M, Vernoux J, Gueguen M, Appl Environ Microbiol 2001 91 1103 1109 10.1046/j.1365-2672.2001.01481.x
45. Safety assessment of dairy microorganisms: the Lactobacillus genus. Bernardeau M, Vernoux J, Henri-Dubernet S, Guéguen M, Int J Food Microbiol 2008 126 278 285 10.1016/j.ijfoodmicro.2007.08.015 17889388
46. Detection and identification of lactic acid bacteria in milk and industrial starter culture with fluorescently labeled rRNA-targeted peptide nucleic acid probes. Matte-Taillez O, Quénée P, Çibik R, Van Opstal J, Dessevre F, Firmesse O, Tailliez P, Lait 2001 81 237 248 10.1051/lait:2001127
47. Response of Gardnerella vaginalis biofilm to 5 days of moxi£oxacin treatment. Swidsinski A, Dorffel Y, Loening-Baucke V, Schilling J, Mendling W, FEMS Immunol Med Microbiol 2011 61 41 46 10.1111/j.1574-695X.2010.00743.x 20955467
48. Selective medium for isolation and enumeration of Bifidobacterium spp. Munoa FJ, Pares R, Appl Environ Microbiol 1988 54 1715 1718 3415235
49. Strong correspondence in bacterial loads between the vagina and rectum of pregnant women. El Aila NA, Tency I, Saerens B, De Backer E, Cools P, dos Santos Santiago GL, Verstraelen H, Verhelst R, Temmerman M, Vaneechoutte M, Res Microbiol 2011 162 506 513 10.1016/j.resmic.2011.04.004 21513795
50. Bifidobacterium spp. and Lactobacillus acidophilus: biological, biochemical, technological and therapeutical properties relevant for use as probiotics. Gomes AMP, Malcata FX, Trends Food Sci. Technol 1999 10 139 157 10.1016/S0924-2244(99)00033-3
51. Group A streptococcal vaginitis: an unrecognized cause of vaginal symptoms in adult women. Verstraelen H, Verhelst R, Vaneechoutte M, Temmerman M, Arch Gynecol Obstet 2011 284 95 8 10.1007/s00404-011-1861-6 21336834
52. DNA mimics for the rapid identification of microorganisms by fluorescence in situ hybridization (FISH). Cerqueira L, Azevedo NF, Almeida C, Jardim T, Keevil C, Vieira MJ, Int J Mol Sci 2008 9 1944 1960 10.3390/ijms9101944 19325728
53. Alloscardovia omnicolens gen. nov., sp. nov., from human clinical samples. Huys G, Vancanneyt M, D'Haene K, Falsen E, Wauters G, Vandamme P, Int J Syst Evol Microbiol 2007 57 1442 1446 10.1099/ijs.0.64812-0 17625172
54. Gardnerella vaginalis isolated from patients with bacterial vaginosis and from patients with healthy vaginal ecosystems. Aroutcheva AA, Simoes JA, Behbakht K, Faro S, Clin Infect Dis 2001 33 1022 1027 10.1086/323030 11528575
55. Longitudinal study of the biotypes of Gardnerella vaginalis. Briselden A, Hillier S, J Clin Microbiol 1990 28 2761 2764 2280007
56. Exploring the diversity of Gardnerella vaginalis in the genitourinary tract microbiota of monogamous couples through subtle nucleotide variation. Eren AM, Zozaya M, Taylor CM, Dowd SE, Martin DH, Ferris MJ, PLoS One 2011 6 26732 e26740 10.1371/journal.pone.0026732 22046340
57. Biotypes and virulence factors of Gardnerella vaginalis isolated from cases of bacterial vaginosis. Udayalaxmi J, Bhat GK, Kotigadde S, Indian J Med Microbiol 2011 29 165 168 10.4103/0255-0857.81798 21654113
58. Drawing the line between commensal and pathogenic Gardnerella vaginalis through genome analysis and virulence studies. Harwich MD, Alves JM, Buck GA, Strauss JF, Patterson JL, Oki AT, Girerd PH, Jefferson KK, BMC Genomics 2010 11 375 386 10.1186/1471-2164-11-375 20540756
59. DNA hybridization test: rapid diagnostic tool for excluding bacterial vaginosis in pregnant women with symptoms suggestive of infection. Witt A, Petricevic L, Kaufmann U, Gregor H, Kiss H, J Clin Microbiol 2002 40 3057 3059 10.1128/JCM.40.8.3057-3059.2002 12149379
60. Quantitative comparison of long-wavelength alexa fluor dyes to Cy dyes: fluorescence of the dyes and their bioconjugates. Berlier JE, Rothe A, Buller G, Bradford J, Gray DR, Filanoski BJ, Telford WG, Yue S, Liu J, Cheung C, Chang W, Hirsch JD, Beechem JM, Haugland RP, J Histochem Cytochem 2003 51 1699 1712 10.1177/002215540305101214 14623938