DOI QR코드

DOI QR Code

Oligotrophic Media Compared with a Tryptic Soy Agar or Broth for the Recovery of Burkholderia cepacia Complex from Different Storage Temperatures and Culture Conditions

  • Ahn, Youngbeom (Division of Microbiology, National Center for Toxicological Research, U.S. Food and Drug Administration) ;
  • Lee, Un Jung (Division of Biochemical Toxicology, National Center for Toxicological Research, U.S. Food and Drug Administration) ;
  • Lee, Yong-Jin (Department of Biological Sciences, Albany State University) ;
  • LiPuma, John J. (Department of Pediatrics, University of Michigan) ;
  • Hussong, David (Eagle Analytical Services) ;
  • Marasa, Bernard (Office of Pharmaceutical Quality, Center for Drug Evaluation and Research, U.S. Food and Drug Administration) ;
  • Cerniglia, Carl E. (Division of Microbiology, National Center for Toxicological Research, U.S. Food and Drug Administration)
  • Received : 2019.06.12
  • Accepted : 2019.08.17
  • Published : 2019.10.28

Abstract

The Burkholderia cepacia complex (BCC) is capable of remaining viable in low-nutrient environments and harsh conditions, posing a contamination risk in non-sterile pharmaceutical products as well as a challenge for detection. To develop optimal recovery methods to detect BCC, three oligotrophic media were evaluated and compared with nutrient media for the recovery of BCC from autoclaved distilled water or antiseptic solutions. Serial dilutions ($10^{-1}$ to $10^{-12}CFU/ml$) of 20 BCC strains were inoculated into autoclaved distilled water and stored at $6^{\circ}C$, $23^{\circ}C$ and $42^{\circ}C$ for 42 days. Six suspensions of Burkholderia cenocepacia were used to inoculate aqueous solutions containing $5{\mu}g/ml$ and $50{\mu}g/ml$ chlorhexidine gluconate (CHX) and $10{\mu}g/ml$ benzalkonium chloride (BZK), and stored at $23^{\circ}C$ for a further 199 days. Nutrient media such as Tryptic Soy Agar (TSA) or Tryptic Soy Broth (TSB), oligotrophic media (1/10 strength TSA or TSB, Reasoner's $2^{nd}$ Agar [R2A] or Reasoner's $2^{nd}$ Broth [R2AB], and 1/3 strength R2A or R2AB) were compared by inoculating these media with BCC from autoclaved distilled water and from antiseptic samples. The recovery of BCC in water or antiseptics was higher in culture broth than on solid media. Oligotrophic medium showed a higher recovery efficiency than TSA or TSB for the detection of 20 BCC samples. Results from multiple comparisons allowed us to directly identify significant differences between TSA or TSB and oligotrophic media. An oligotrophic medium pre-enrichment resuscitation step is offered for the United States Pharmacopeia (USP) proposed compendial test method for BCC detection.

Keywords

References

  1. DSMZ. 2019. Prokaryotic nomenclature up-to-date. Available from https://www.dsmz.de/bacterial-diversity/prokaryoticnomenclature-up-to-date/prokaryotic-nomenclature-up-to-date.html. Accessed May 17, 2019.
  2. Peeters C, Zlosnik JEA, Spilker T, Hird TJ, LiPuma JJ, Vandamme P. 2013. Burkholderia pseudornultivorans sp nov., a novel Burkholderia cepacia complex species from human respiratory samples and the rhizosphere. Syst. Appl. Microbiol. 36: 483-489. https://doi.org/10.1016/j.syapm.2013.06.003
  3. Ahn Y, Kim JM, Kweon O, Kim SJ, Jones RC, Woodling K, et al. 2016. Intrinsic resistance of Burkholderia cepacia complex to benzalkonium chloride. MBio. 7: e01716.
  4. Martina P, Leguizamon M, Prieto CI, Sousa SA, Montanaro P, Draghi WO, et al. 2018. Burkholderia puraquae sp. nov., a novel species of the Burkholderia cepacia complex isolated from hospital settings and agricultural soils. Int. J. Syst. Evol. Microbiol. 68: 14-20. https://doi.org/10.1099/ijsem.0.002293
  5. Peeters C, Meier-Kolthoff JP, Verheyde B, De Brandt E, Cooper VS, Vandamme P. 2016. Phylogenomic study of Burkholderia glathei-like organisms, proposal of 13 novel Burkholderia species and emended descriptions of Burkholderia sordidicola, Burkholderia zhejiangensis, and Burkholderia grimmiae. Front Microbiol. 7: 877.
  6. Mahenthiralingam E, Baldwin A, Dowson CG. 2008. Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J. Appl. Microbiol. 104: 1539-1551. https://doi.org/10.1111/j.1365-2672.2007.03706.x
  7. FDA. 2017. FDA updates on 2017 Burkholderia cepacia contamination. Available from https://www.fda.gov/Drugs/DrugSafety/ucm570672.htm. Accessed May 17, 2019.
  8. FDA. 2017. FDA advises drug manufacturers that Burkholderia cepacia complex poses a contamination risk in non-sterile, water-based drug products. Available from https://www.fda.gov/Drugs/DrugSafety/ucm559508.htm. Accessed May 17, 2019.
  9. CDC. 2017. Multistate outbreak of Burkholderia cepacia infections associated with oral liquid docusate sodium. Available from https://www.cdc.gov/hai/outbreaks/bcepacia/. Accessed May 17, 2019.
  10. CDC. 2017. Multistate outbreak of Burkholderia cepacia bloodstream infections associated with contaminated prefilled saline flush syringes. Available from https://www.cdc.gov/hai/outbreaks/b-cepacia-saline-flush/index.html. Accessed May 17, 2019.
  11. CDC. 2018. Multistate outbreak of Burkholderia cepacia complex infections associated with the use of medline remedy essentials no-rinse cleaning foam. Available from https://www.cdc.gov/hai/outbreaks/b-cepacia/no-rinse.html. Accessed May 17, 2019.
  12. Becker SL, Berger FK, Feldner SK, Karliova I, Haber M, Mellmann A, et al. 2018. Outbreak of Burkholderia cepacia complex infections associated with contaminated octenidine mouthwash solution, Germany, August to September 2018. Euro. Surveill. 23: 1800540.
  13. Torbeck L RD, Guilfoyle DE, Friedman RL, Hussong D. 2011. Burkholderia cepacia: This decision is overdue. PDA J. Pharm. Sci. Technol. 65: 535-543. https://doi.org/10.5731/pdajpst.2011.00793
  14. Jimenez L. 2007. Microbial diversity in pharmaceutical product recalls and environments. PDA J. Pharm. Sci. Technol. 61: 383-399.
  15. Robertson J, Levy A, Sagripanti JL, Inglis TJJ. 2010. The Survival of Burkholderia pseudomallei in Liquid Media. Am. J. Trop. Med. Hyg. 82: 88-94. https://doi.org/10.4269/ajtmh.2010.09-0226
  16. Kim JM, Ahn Y, LiPuma JJ, Hussong D, Cerniglia CE. 2015. Survival and susceptibility of Burkholderia cepacia complex in chlorhexidine gluconate and benzalkonium chloride. J. Ind. Microbiol. Biotechnol. 42: 905-913. https://doi.org/10.1007/s10295-015-1605-x
  17. Gilligan PH, Whittier S. 1999. Burkholderia, Stenotrophomonas, Ralstonia, Brevundimonas, Comamonas, and Acidovorax, pp. 526-538. In Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH (eds.), Manual of clinical microbiology, 7th ed. American Society for Microbiology, Washington, D.C.
  18. Carson LA, Favero MS, Bond WW, Petersen NJ. 1973. Morphological, biochemical, and growth characteristics of Pseudomonas cepacia from distilled water. Appl. Microbiol. 25: 476-483. https://doi.org/10.1128/AEM.25.3.476-483.1973
  19. Chiarini L, Bevivino A, Dalmastri C, Tabacchioni S, Visca P. 2006. Burkholderia cepacia complex species: health hazards and biotechnological potential. Trends Microbiol. 14: 277-286. https://doi.org/10.1016/j.tim.2006.04.006
  20. Ahn Y, Kim JM, Ahn H, Lee YJ, LiPuma J, Hussong D, et al. 2014. Evaluation of liquid and solid culture media for the recovery and enrichment of Burkholderia cenocepacia from distilled water J. Ind. Microbiol. Biotechnol. 41: 1109-1118. https://doi.org/10.1007/s10295-014-1442-3
  21. Ahn Y, Kim JM, Lee YJ, LiPuma J, Hussong D, Marasa B, et al. 2017. Effects of extended storage of chlorhexidine gluconate and benzalkonium chloride solutions on the viability of Burkholderia cenocepacia. J. Microbiol. Biotechnol. 27: 2211-2220. https://doi.org/10.4014/jmb.1706.06034
  22. USP. 2016. <1111> Microbiological examination of non-sterile products: acceptance criteria for pharmaceutical preparations and substances for pharmaceutical use. Available from https://www.usp.org/sites/default/files/usp/document/harmonization/gen-method/q05c_pf_ira_33_2_2007.pdf. Accessed May 17, 2019.
  23. USP. 2016. <61> Microbiological examination of nonsterile products - microbial enumeration tests. Available from https://hmc.usp.org/sites/default/files/documents/HMC/GCs-Pdfs/c61.pdf. Accessed May 17, 2019.
  24. USP. 2016. <62> Microbiological examination of nonsterile products - tests for specified microorganisms. Available from https://www.usp.org/sites/default/files/usp/document/harmonization/gen-method/q05a_pf_ira_34_6_2008.pdf. Accessed May 17, 2019.
  25. Vanlaere E, Coenye T, Samyn E, Van den Plas C, Govan J, De Baets F, et al. 2005. A novel strategy for the isolation and identification of environmental Burkholderia cepacia complex bacteria. FEMS Microbiol. Lett. 249: 303-307. https://doi.org/10.1016/j.femsle.2005.06.026
  26. Vermis K, Brachkova M, Vandamme P, Nelis H. 2003. Isolation of Burkholderia cepacia complex genomovars from waters. Syst. Appl. Microbiol. 26: 595-600. https://doi.org/10.1078/072320203770865909
  27. Carson LA, Tablan OC, Cusick LB, Jarvis WR, Favero MS, Bland LA. 1988. Comparative evaluation of selective media for isolation of Pseudomonas cepacia from cystic fibrosis patients and environmental sources. J. Clin. Microbiol. 26: 2096-2100. https://doi.org/10.1128/JCM.26.10.2096-2100.1988
  28. Kawai M, Matsutera E, Kanda H, Yamaguchi N, Tani K, Nasu M. 2002. 16S ribosomal DNA-based analysis of bacterial diversity in purified water used in pharmaceutical manufacturing processes by PCR and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 68: 699-704. https://doi.org/10.1128/AEM.68.2.699-704.2002
  29. Nagarkar PP, Ravetkar SD, Watve MG. 2001. Oligophilic bacteria as tools to monitor aseptic pharmaceutical production units. Appl. Environ. Microbiol. 67: 1371-1374. https://doi.org/10.1128/AEM.67.3.1371-1374.2001
  30. Venkateswaran K, Hattori N, La Duc MT, Kern R. 2003. ATP as a biomarker of viable microorganisms in clean-room facilities. J. Microbiol. Methods. 52: 367-377. https://doi.org/10.1016/S0167-7012(02)00192-6
  31. Kulakov LA, McAlister MB, Ogden KL, Larkin MJ, O'Hanlon JF. 2002. Analysis of bacteria contaminating ultrapure water in industrial systems. Appl. Environ. Microbiol. 68: 1548-1555. https://doi.org/10.1128/AEM.68.4.1548-1555.2002
  32. Baranyi J, Roberts TA. 1994. A dynamic approach to predicting bacterial growth in food. Int. J. Food Microbiol. 23: 277-294. https://doi.org/10.1016/0168-1605(94)90157-0
  33. Cassidy MB, Leung KT, Lee H, Trevors JT. 2000. A comparison of enumeration methods for culturable Pseudomonas fluorescens cells marked with green fluorescent protein. J. Microbiol. Methods 40: 135-145. https://doi.org/10.1016/S0167-7012(99)00131-1
  34. Jin M, Wang B. 2014. Implementing multiple comparisons on pearson chi-square test for an R$\times$C contingency table in SAS. SAS Global Forum Proc. 1544: 1541-1546
  35. Schaffter N, Parriaux A. 2002. Pathogenic-bacterial water contamination in mountainous catchments. Water Res. 36: 131-139. https://doi.org/10.1016/S0043-1354(01)00242-1
  36. Pumpuang A, Chantratita N, Wikraiphat C, Saiprom N, Day NPJ, Peacock SJ, et al. 2011. Survival of Burkholderia pseudomallei in distilled water for 16 years. Trans. R. Soc. Trop. Med. Hyg. 105: 598-600. https://doi.org/10.1016/j.trstmh.2011.06.004
  37. Gilbert SE, Rose LJ. 2012. Survival and persistence of nonspore-forming biothreat agents in water. Lett. Appl. Microbiol. 55: 189-194. https://doi.org/10.1111/j.1472-765X.2012.03277.x
  38. Moore RA, Tuanyok A, Woods DE. 2008. Survival of Burkholderia pseudomallei in water. BMC Res. Notes 1: 11. https://doi.org/10.1186/1756-0500-1-11
  39. Moore JE, Nagano Y, Millar BC, McCalmont M, Elborn JS, Rendall J, et al. 2007. Environmental persistence of Pseudomonas aeruginosa and Burkholderia multivorans in sea water: preliminary evidence of a viable but non-culturable state. Br. J. Biomed. Sci. 64: 129-131. https://doi.org/10.1080/09674845.2007.11978100
  40. Tong S, Yang S, Lu Z, He W. 1996. Laboratory investigation of ecological factors influencing the environmental presence of Burkholderia pseudomallei. Microbiol. Immunol. 40: 451-453. https://doi.org/10.1111/j.1348-0421.1996.tb01092.x
  41. ASTM. 2012. ASTM F1094 - 87, Standard test methods for microbiological monitoring of water used for processing electron and microelectronic devices by direct pressure tap sampling valve and by the presterilized plastic bag method. Available from www.astm.org. Accessed May 17, 2019.
  42. Hagedorn C, Gould WD, Bardinelli TR, Gustavson DR. 1987. A selective medium for enumeration and recovery of Pseudomonas cepacia biotypes from soil. Appl. Environ. Microbiol. 53: 2265-2268. https://doi.org/10.1128/AEM.53.9.2265-2268.1987
  43. Peeters C, Depoorter E, Praet J, Vandamme P. 2016. Extensive cultivation of soil and water samples yields various pathogens in patients with cystic fibrosis but not Burkholderia multivorans. J. Cyst. Fibros. 15: 769-775. https://doi.org/10.1016/j.jcf.2016.02.014
  44. Mitchell AJ, Wimpenny JW. 1997. The effects of agar concentration on the growth and morphology of submerged colonies of motile and non-motile bacteria. J. Appl. Microbiol. 83: 76-84. https://doi.org/10.1046/j.1365-2672.1997.00192.x
  45. Pharmawebinars. 2019. New proposed general chapter USP <60> Microbiological examination of nonsterile products - tests for Burkholderia cepacia complex. Available from https://www.pharmawebinars.com/usp-60-tests-for-burkholderiacepacia-complex. Accessed May 17, 2019.

Cited by

  1. A comparison of culture-based, real-time PCR, droplet digital PCR and flow cytometric methods for the detection of Burkholderia cepacia complex in nuclease-free water and antiseptics vol.47, pp.6, 2019, https://doi.org/10.1007/s10295-020-02287-3
  2. Loop-Mediated Isothermal Amplification (LAMP) Assay for Detecting Burkholderia cepacia Complex in Non-Sterile Pharmaceutical Products vol.10, pp.9, 2019, https://doi.org/10.3390/pathogens10091071