Improved sensitivity for molecular detection of bacterial and candida infections in blood

Journal of Clinical Microbiology

Volumn 52, Issue 9, 2014, Pages 3164-3174

  Bacconi, Andrea ^a   Richmond, Gregory S ^a   Baroldi, Michelle A ^a   Laffler, Thomas G ^a   Blyn, Lawrence B ^a   Carolan, Heather E ^a   Frinder, Mark R ^a   Toleno, Donna M ^a   Metzgar, David ^a   Gutierrez, Jose R ^a   Massire, Christian ^a   Rounds, Megan ^a   Kennel, Natalie J ^a   Rothman, Richard E ^b   Peterson, Stephen ^b   Carroll, Karen C ^c   Wakefield, Teresa ^c   Ecker, David J ^a   Sampath, Rangarajan ^a  

^a Ibis Biosciences Inc   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; BACTEREMIA; BLOOD; CANDIDEMIA; ELECTROSPRAY MASS SPECTROMETRY; EVALUATION STUDY; FEMALE; HUMAN; LABORATORY AUTOMATION; LABORATORY DIAGNOSIS; MALE; MICROBIOLOGY; MOLECULAR DIAGNOSIS; POLYMERASE CHAIN REACTION; PROCEDURES; PROSPECTIVE STUDY; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

ADOLESCENT; ADULT; AUTOMATION, LABORATORY; BACTEREMIA; BLOOD; CANDIDEMIA; FEMALE; HUMANS; MALE; MOLECULAR DIAGNOSTIC TECHNIQUES; POLYMERASE CHAIN REACTION; PROSPECTIVE STUDIES; SENSITIVITY AND SPECIFICITY; SPECIMEN HANDLING; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; YOUNG ADULT;

EID: 84906857817     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.00801-14     Document Type: Article

References (59)

1. Kumar A, Roberts D, Wood KE, Light B, Parrillo JE, Sharma S, Suppes R, Feinstein D, Zanotti S, Taiberg L, Gurka D, Kumar A, Cheang M. 2006. Duration of hypotension before initiation of effective antimicrobial therapy is the critical determinant of survival in human septic shock. Crit. Care Med. 34: 1589-1596. http://dx.doi.org/10.1097/01.CCM.0000217961.75225.E9. (Pubitemid 43810035)
2. Dellinger RP, Levy MM, Rhodes A, Annane D, Gerlach H, Opal SM, Sevransky JE, Sprung CL, Douglas IS, Jaeschke R, Osborn TM, Nunnally ME, Townsend SR, Reinhart K, Kleinpell RM, Angus DC, Deutschman CS, Machado FR, Rubenfeld GD, Webb SA, Beale RJ, Vincent JL, Moreno R, Surviving Sepsis Campaign Guidelines Committee including the Pediatric Subgroup. 2013. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2012. Crit. Care Med. 41:580-637. http://dx.doi.org/10.1097/CCM.0b013e31827e83af.
3. Dellinger RP, Levy MM, Carlet JM, Bion J, Parker MM, Jaeschke R, Reinhart K, Angus DC, Brun-Buisson C, Beale R, Calandra T, Dhainaut JF, Gerlach H, Harvey M, Marini JJ, Marshall J, Ranieri M, Ramsay G, Sevransky J, Thompson BT, Townsend S, Vender JS, Zimmerman JL, Vincent JL, International Surviving Sepsis Campaign Guidelines Committee, American Association of Critical-Care Nurses, American College of Chest Physicians, American College of Emergency Physicians, Canadian Critical Care Society, European Society of Clinical Microbiology and Infectious Diseases, European Society of Intensive Care Medicine, European Respiratory Society, International Sepsis Forum, Japanese Association for Acute Medicine, Japanese Society of Intensive Care Medicine, Society of Critical Care Medicine, Society of Hospital Medicine, Surgical Infection Society, World Federation of Societies of Intensive and Critical Care Medicine. 2008. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit. Care Med. 36:296-327. http://dx.doi.org/10.1097/01. CCM.0000298158.12101.41.
4. Kuti EL, Patel AA, Coleman CI. 2008. Impact of inappropriate antibiotic therapy on mortality in patients with ventilator-associated pneumonia and blood stream infection: a meta-analysis. J. Crit. Care. 23:91-100. http://dx.doi.org/10.1016/j.jcrc.2007.08.007. (Pubitemid 351400347)
5. Kollef MH. 2008. Broad-spectrum antimicrobials and the treatment of serious bacterial infections: getting it right up front. Clin. Infect. Dis. 47(Suppl 1):S3-S13. http://dx.doi.org/10.1086/590061.
6. Fenollar F, Raoult D. 2007. Molecular diagnosis of bloodstream infections caused by non-cultivable bacteria. Int. J. Antimicrob. Agents 30(Suppl 1):S7-S15. http://dx.doi.org/10.1016/j.ijantimicag.2007.06.024.
7. Rangel-Frausto MS, Pittet D, Costigan M, Hwang T, Davis CS, Wenzel RP. 1995. The natural history of the systemic inflammatory response syndrome (SIRS). A prospective study. JAMA 273:117-123.
8. Lamy B, Roy P, Carret G, Flandrois JP, Delignette-Muller ML. 2002. What is the relevance of obtaining multiple blood samples for culture? A comprehensive model to optimize the strategy for diagnosing bacteremia. CID. 35:842-850. http://dx.doi.org/10.1086/342383.
9. Reimer LG, Wilson ML, Weinstein MP. 1997. Update on detection of bacteremia and fungemia. Clin. Microbiol. Rev. 10:444-465. (Pubitemid 27359260)
10. Weinstein MP. 1996. Current blood culture methods and systems: clinical concepts, technology, and interpretation of results. Clin. Infect. Dis. 23: 40-46. http://dx.doi.org/10.1093/clinids/23.1.40. (Pubitemid 26323793)
11. Morata P, Queipo-Ortuño MI, de Dios Colmenero J. 1998. Strategy for optimizing DNA amplification in a peripheral blood PCR assay used for diagnosis of human brucellosis. J. Clin. Microbiol. 36:2443-2446.
12. Cogswell FB, Bantar CE, Hughes TG, Gu Y, Philipp MT. 1996. Host DNA can interfere with detection of Borrelia burgdorferi in skin biopsy specimens by PCR. J. Clin. Microbiol. 34:980-982. (Pubitemid 26091522)
13. Peters RP, van Agtmael MA, Gierveld S, Danner SA, Groeneveld AB, Vandenbroucke-Grauls CM, Savelkoul PH. 2007. Quantitative detection of Staphylococcus aureus and Enterococcus faecalis DNA in blood to diagnose bacteremia in patients in the intensive care unit. J. Clin. Microbiol. 45:3641-3646. http://dx.doi.org/10.1128/JCM.01056-07. (Pubitemid 350156861)
14. Handschur M, Karlic H, Hertel C, Pfeilstöcker M, Haslberger AG. 2009. Preanalytic removal of human DNA eliminates false signals in general 16S rDNA PCR monitoring of bacterial pathogens in blood. Comp. Immunol. Microbiol. Infect. Dis. 32:207-219. http://dx.doi.org/10.1016/j.cimid.2007.10.005.
15. Gebert S, Siegel D, Wellinghausen N. 2008. Rapid detection of pathogens in blood culture bottles by real-time PCR in conjunction with the preanalytic tool MolYsis. J. Infect. 57:307-316. http://dx.doi.org/10.1016/j.jinf.2008.07. 013.
16. Hansen WL, Bruggeman CA, Wolffs PF. 2009. Evaluation of new pre-analysis sample treatment tools and DNA isolation protocols to improve bacterial pathogen detection in whole blood. J. Clin. Microbiol. 47:2629-2631. http://dx.doi.org/10.1128/JCM.00821-09.
17. Wellinghausen N, Kochem AJ, Disqué C, Mühl H, Gebert S, Winter J, Matten J, Sakka SG. 2009. Diagnosis of bacteremia in whole-blood samples by use of a commercial universal 16S rRNA gene-based PCR and sequence analysis. J. Clin. Microbiol. 47:2759-2765. http://dx.doi.org/10.1128/JCM.00567- 09.
18. Sachse S, Straube E, Lehmann M, Bauer M, Russwurm S, Schmidt KH. 2009. Truncated human cytidylate-phosphate-deoxyguanylate-binding protein for improved nucleic acid amplification technique-based detection of bacterial species in human samples. J. Clin. Microbiol. 47:1050-1057. http://dx.doi.org/10.1128/JCM. 02242-08.
19. Lehmann LE, Alvarez J, Hunfeld KP, Goglio A, Kost GJ, Louie RF, Raglio A, Regueiro BJ, Wissing H, Stüber F. 2009. Potential clinical utility of polymerase chain reaction in microbiological testing for sepsis. Crit. Care Med. 37:3085-3090. http://dx.doi.org/10.1097/CCM.0b013e3181b033d7.
20. Schreiber J, Nierhaus A, Braune SA, de Heer G, Kluge S. 2013. Comparison of three different commercial PCR assays for the detection of pathogens in critically ill sepsis patients. Med. Klin. Intensivmed. Notfmed. 108:311-318. http://dx.doi.org/10.1007/s00063-013-0227-1.
21. Ecker DJ, Sampath R, Li H, Massire C, Matthews HE, Toleno D, Hall TA, Blyn LB, Eshoo MW, Ranken R, Hofstadler SA, Tang YW. 2010. New technology for rapid molecular diagnosis of bloodstream infections. Expert Rev. Mol. Diagn. 10:399-415. http://dx.doi.org/10.1586/erm.10.24.
22. Kaleta EJ, Clark AE, Cherkaoui A, Wysocki VH, Ingram EL, Schrenzel J, Wolk DM. 2011. Comparative analysis of PCR-electrospray ionization/ mass spectrometry (MS) and MALDI-TOF/MS for the identification of bacteria and yeast from positive blood culture bottles. Clin. Chem. 57: 1057-1067. http://dx.doi.org/10.1373/clinchem.2011.161968.
23. Kaleta EJ, Clark AE, Johnson DR, Gamage DC, Wysocki VH, Cherkaoui A, Schrenzel J, Wolk DM. 2011. Use of PCR coupled with electrospray ionization mass spectrometry for rapid identification of bacterial and yeast bloodstream pathogens from blood culture bottles. J. Clin. Microbiol. 49:345-353. http://dx.doi.org/10.1128/JCM.00936-10.
24. Metzgar D, Frinder M, Lovari R, Toleno D, Massire C, Blyn LB, Ranken R, Carolan HE, Hall TA, Moore D, Hansen CJ, Sampath R, Ecker DJ. 2013. Broad-spectrum biosensor capable of detecting and identifying diverse bacterial and Candida species in blood. J. Clin. Microbiol. 51:2670-2678. http://dx.doi.org/10.1128/JCM.00966-13.
25. Eshoo MW, Crowder CD, Li H, Matthews HE, Meng S, Sefers SE, Sampath R, Stratton CW, Blyn LB, Ecker DJ, Tang YW. 2010. Detection and identification of Ehrlichia species in blood by use of PCR and electrospray ionization mass spectrometry. J. Clin. Microbiol. 48:472-478. http://dx.doi.org/10.1128/JCM. 01669-09.
26. Crowder CD, Matthews H, Schutzer S, Rounds MA, Luft BJ, Nolte O, Campbell SR, Phillipson CA, Li F, Sampath R, Ecker DJ, Eshoo MW. 2010. Genotypic variation and mixtures of Lyme Borrelia in Ixodes ticks from North America and Europe. PLoS One 5:e10650. http://dx.doi.org/10.1371/journal.pone.0010650.
27. Farrell JJ, Sampath R, Bonomo RA. 2011. Identifying pathogens in "culture negative" infections: a case series exploring PCR and electrospray ionization mass spectrometry for microbial identification; poster 1022. Annual Meeting of the Infectious Diseases Society of America, Boston, MA, 20 to 23 October 2011.
28. Laffler TG, Cummins LL, McClain CM, Quinn CD, Toro MA, Carolan HE, Toleno DM, Rounds MA, Eshoo M, Stratton CW, Sampath R, Blyn LB, Ecker DJ, Tang YW. 2013. Enhanced diagnostic yields of bacteremia and candidemia in blood specimens by PCR/electrospray ionization mass spectrometry. J. Clin. Microbiol. 51:3535-3541. http://dx.doi.org/10.1128/JCM.00876-13.
29. Jordana-Lluch E, Carolan HE, Giménez M, Sampath R, Ecker DJ, Quesada MD, Modol JM, Arméstar F, Blyn LB, Cummins LL, Ausina V, Martró E. 2013. Rapid diagnosis of bloodstream infections with PCR followed by mass spectrometry. PLoS One 8:e62108. http://dx.doi.org/10.1371/ journal.pone.0062108.
30. Hofstadler SA, Sampath R, Blyn LB, Eshoo MW, Hall TA, Jiang Y, Drader JJ, Hannis JC, Sannes-Lowery KA, Cummins LL, Libby B, Walcott DJ, Schink A, Massire C, Ranken R, Gutierrez J, Manalili S, Ivy C, Melton R, Levene H, Barrett-Wilt G, Feng L, Zapp V, White N, Samant V, McNeil JA, Knize D, Robbins D, Rudnik K, Desai A, Moradi E, Ecker DJ. 2005. TIGER: the universal biosensor. Int. J. Mass Spectrom. 242:23-41. http://dx.doi.org/10.1016/j.ijms.2004.09.014. (Pubitemid 40297903)
31. CLSI. 2008. Interpretive criteria for identification of bacteria and fungi by DNA target sequencing; approved guideline. CLSI Document MM18-A. Clinical and Laboratory Standards Institute, Wayne, PA.
32. Bowers DR, Hunter AS, Jacobs DM, Kuper KM, Musick WL, Perez KK, Shah DN, Schilling AN. 2013. Significant publications on infectious diseases pharmacotherapy in 2012. Am. J. Health Syst. Pharm. 70:1930-1940. http://dx.doi.org/10.2146/ajhp130129.
33. Chuang YC, Chang SC, Wang WK. 2012. Using the rate of bacterial clearance determined by real-time polymerase chain reaction as a timely surrogate marker to evaluate the appropriateness of antibiotic usage in critical patients with Acinetobacter baumannii bacteremia. Crit. Care Med. 40:2273-2280. http://dx.doi.org/10.1097/CCM.0b013e3182515190.
34. Agampodi SB, Matthias MA, Moreno AC, Vinetz JM. 2012. Utility of quantitative polymerase chain reaction in leptospirosis diagnosis: association of level of leptospiremia and clinical manifestations in Sri Lanka. Clin. Infect. Dis. 54:1249-1255. http://dx.doi.org/10.1093/cid/cis035.
35. Darton T, Guiver M, Naylor S, Jack DL, Kaczmarski EB, Borrow R, Read RC. 2009. Severity of meningococcal disease associated with genomic bacterial load. Clin. Infect. Dis. 48:587-594. http://dx.doi.org/10.1086/596707.
36. Massi MN, Shirakawa T, Gotoh A, Bishnu A, Hatta M, Kawabata M. 2005. Quantitative detection of Salmonella enterica serovar Typhi from blood of suspected typhoid fever patients by real-time PCR. Int. J. Med. Microbiol. 295:117-120. http://dx.doi.org/10.1016/j.ijmm.2005.01.003. (Pubitemid 40692863)
37. Kirkbright S, Fatovich D, Kee C, Kay I, Flexman J, Pryce TM, Waterer GW. 2011. Quantitative rt-PCR holds promise as a screening tool for patients with severe sepsis. Emerg. Med. Australas. 23:502-506. http://dx.doi.org/10.1111/j. 1742-6723.2011.01445.x.
38. Reier-Nilsen T, Farstad T, Nakstad B, Lauvrak V, Steinbakk M. 2009. Comparison of broad range 16S rDNA PCR and conventional blood culture for diagnosis of sepsis in the newborn: a case control study. BMC Pediatr. 9:5. http://dx.doi.org/10.1186/1471-2431-9-5.
39. Chuang YC, Chang SC, Wang WK. 2010. High and increasing Oxa-51 DNA load predict mortality in Acinetobacter baumannii bacteremia: implication for pathogenesis and evaluation of therapy. PLoS One 5:e14133. http://dx.doi.org/10. 1371/journal.pone.0014133.
40. Reller ME, Clemens EG, Schachterle SE, Mtove GA, Sullivan DJ, Dumler JS. 2011. Multiplex 5= nuclease-quantitative PCR for diagnosis of relapsing fever in a large Tanzanian cohort. J. Clin. Microbiol. 49:3245-3249. http://dx.doi.org/10.1128/JCM.00940-11.
41. Ho YC, Chang SC, Lin SR, Wang WK. 2009. High levels of mecA DNA detected by a quantitative real-time PCR assay are associated with mortality in patients with methicillin-resistant Staphylococcus aureus bacteremia. J. Clin. Microbiol. 47:1443-1451. http://dx.doi.org/10.1128/JCM.01197-08.
42. Rello J, Lisboa T, Lujan M, Gallego M, Kee C, Kay I, Lopez D, Waterer GW, DNA-Neumococo Study Group. 2009. Severity of pneumococcal pneumonia associated with genomic bacterial load. Chest 136:832-840. http://dx.doi.org/10.1378/chest. 09-0258.
43. Navarro E, Segura JC, Castaño MJ, Solera J. 2006. Use of real-time quantitative polymerase chain reaction to monitor the evolution of Brucella melitensis DNA load during therapy and post-therapy follow-up in patients with brucellosis. Clin. Infect. Dis. 42:1266-1273. http://dx.doi.org/10.1086/503035.
44. Peters RP, de Boer RF, Schuurman T, Gierveld S, Kooistra-Smid M, van Agtmael MA, Vandenbroucke-Grauls CM, Persoons MC, Savelkoul PH. 2009. Streptococcus pneumoniae DNA load in blood as a marker of infection in patients with community-acquired pneumonia. J. Clin. Microbiol. 47:3308-3312. http://dx.doi.org/10.1128/JCM.01071-09.
45. Kee C, Palladino S, Kay I, Pryce TM, Murray R, Rello J, Gallego M, Lujan M, Muñoz-Almagro C, Waterer GW. 2008. Feasibility of real-time polymerase chain reaction in whole blood to identify Streptococcus pneumoniae in patients with community-acquired pneumonia. Diagn. Microbiol. Infect. Dis. 61: 72-75. http://dx.doi.org/10.1016/j.diagmicrobio.2007.12.011.
46. Kee C, Fatovich DM, Palladino S, Kay ID, Pryce TM, Flexman J, Murray R, Waterer GW. 2010. Specificity of a quantitative real-time polymerase chain reaction assay for the detection of invasive pneumococcal disease: identifying Streptococcus pneumoniae using quantitative polymerase chain reaction. Chest 137:243-244. http://dx.doi.org/10.1378/chest.09-2185.
47. van Haeften R, Palladino S, Kay I, Keil T, Heath C, Waterer GW. 2003. A quantitative LightCycler PCR to detect Streptococcus pneumoniae in blood and CSF. Diagn. Microbiol. Infect. Dis. 47:407-414. http://dx.doi.org/10.1016/S0732- 8893(03)00129-9. (Pubitemid 38373412)
48. Carrol ED, Guiver M, Nkhoma S, Mankhambo LA, Marsh J, Balmer P, Banda DL, Jeffers G, IPD Study Group, White SA, Molyneux EM, Molyneux ME, Smyth RL, Hart CA. 2007. High pneumococcal DNA loads are associated with mortality in Malawian children with invasive pneumococcal disease. The Pediatric Infectious Disease J. 26:416-422. http://dx.doi.org/10.1097/01.inf.0000260253.22994.61.
49. Werner AS, Cobbs CG, Kaye D, Hook EW. 1967. Studies on the bacteremia of bacterial endocarditis. JAMA 202:199-203. http://dx.doi.org/10.1001/jama.1967. 03130160073013.
50. Kreger BE, Craven DE, Carling PC, McCabe WR. 1980. Gram-negative bacteremia. III. Reassessment of etiology, epidemiology and ecology in 612 patients. Am. J. Med. 68:332-343. (Pubitemid 10130373)
51. Henry NK, McLimans CA, Wright AJ, Thompson RL, Wilson WR, Washington JA, Jr. 1983. Microbiological and clinical evaluation of the isolator lysis-centrifugation blood culture tube. J. Clin. Microbiol. 17: 864-869. (Pubitemid 13089665)
52. Waterer G, Rello J. 2011. Why should we measure bacterial load when treating community-acquired pneumonia? Curr. Opin. Infect. Dis. 24: 137-141. http://dx.doi.org/10.1097/QCO.0b013e328343b70d.
53. Øvstebø R, Brandtzaeg P, Brusletto B, Haug KBF, Lande K, Høiby EA, Kierulf P. 2004. Use of robotized DNA isolation and real-time PCR to quantify and identify close correlation between levels of Neisseria meningitidis DNA and lipopolysaccharides in plasma and cerebrospinal fluid from patients with systemic meningococcal disease. J. Clin. Microbiol. 42:2980-2987. http://dx.doi.org/10.1128/JCM.42.7.2980-2987.2004.
54. Perez KK, Olsen RJ, Musick WL, Cernoch PL, Davis JR, Land GA, Peterson LE, Musser JM. 2013. Integrating rapid pathogen identification and antimicrobial stewardship significantly decreases hospital costs. Arch. Pathol. Lab. Med. 137:1247-1254.
55. Huang AM, Newton D, Kunapuli A, Gandhi TN, Washer LL, Isip J, Collins CD, Nagel JL. 2013. Impact of rapid organism identification via matrix-assisted laser desorption/ionization time-of-flight combined with antimicrobial stewardship team intervention in adult patients with bacteremia and candidemia. Clin. Infect. Dis. 57:1237-1245. http://dx.doi.org/10.1093/cid/cit498.
56. Davies J, Gordon CL, Tong SYC, Baird RW, Davis JS. 2012. Impact of results of a rapid Staphylococcus aureus diagnostic test on prescribing of antibiotics for patients with clustered Gram-positive cocci in blood cultures. J. Clin. Microbiol. 50:2056-2058. http://dx.doi.org/10.1128/JCM.06773-11.
57. Sango A, McCarter YS, Johnson D, Ferreira J, Guzman N, Jankowski CA. 2013. Stewardship approach for optimizing antimicrobial therapy through use of a rapid microarray assay on blood cultures positive for Enterococcus species. J. Clin. Microbiol. 51:4008-4011. http://dx.doi.org/10.1128/JCM.01951-13.
58. Farrell JJ, Sampath R, Ecker D, Bonomo RA. 2013. "Salvage microbiology": detection of bacteria directly from clinical specimens following initiation of antimicrobial treatment. PLoS One 8:e66349. http://dx.doi.org/10.1371/journal.pone.0066349.
59. Farrell JJ, Tsung AJ, Flier L, Martinez DL, Beam SB, Chen C, Lowery KS, Sampath R, Bonomo RA. 2013. PCR and electrospray ionizationmass spectrometry (PCR/ESI-MS): detection of persistent Enterococcus faecalis in cerebrospinal fluid following treatment of post-operative ventriculitis. J. Clin. Microbiol. 51:3464-3466. http://dx.doi.org/10.1128/JCM.01343-13. Diseases