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Volume 30, Number 10—October 2024
Research

Virulence of Burkholderia pseudomallei ATS2021 Unintentionally Imported to United States in Aromatherapy Spray

Christopher K. CoteComments to Author , Kevin D. Mlynek, Christopher P. Klimko, Sergei S. Biryukov, Sherry Mou, Melissa Hunter, Nathaniel O. Rill, Jennifer L. Dankmeyer, Jeremey A. Miller, Yuli Talyansky, Michael L. Davies, J. Matthew Meinig, Stephanie A. Halasohoris, Anette M. Gray, Jade L. Spencer, Ashley L. Babyak, M. Kelly Hourihan, Bobby J. Curry, Ronald G. Toothman, Sara I. Ruiz, Xiankun Zeng, Keersten M. Ricks, Tamara L. Clements, Christina E. Douglas, Suma Ravulapalli, Christopher P. Stefan, Charles J. Shoemaker, Mindy G. Elrod, Jay E. Gee, Zachary P. Weiner, Ju Qiu, Joel A. Bozue, Nancy A. Twenhafel, and David DeShazerComments to Author 
Author affiliations: United States Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, Maryland, USA (C.K. Cote, K.D. Mlynek, C.P. Klimko, S.S. Biryukov, S. Mou, M. Hunter, N.O. Rill, J.L. Dankmeyer, J.A. Miller, Y. Talyansky, M.L. Davies, J.M. Meinig, S.A. Halasohoris, A.M. Gray, J.L. Spencer, A.L. Babyak, M.K. Hourihan, B.J. Curry, R.G. Toothman, S.I. Ruiz, X. Zeng, K.M. Ricks, T.L. Clements, C.E. Douglas, S. Ravulapalli, C.P. Stefan, C.J. Shoemaker, J. Qiu, J.A. Bozue, N.A. Twenhafel, D. DeShazer); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (M.G. Elrod, J.E. Gee, Z.P. Weiner)

Main Article

Figure 1

Phylogenetic tree based on bimABp and bimABm alleles from strains of Burkholderia pseudomallei, B. mallei, and B. humptydooensis, showing location of B. mallei ATS2021 (arrow), the causative strain in an an outbreak of 4 cases, 2 of them fatal, in the United States in 2021. NGPhylogeny.fr (12) was used to build the tree in “A la Carte” mode, and it used MUSCLE for multiple alignment, Gblocks for automatic alignment curation (https://NGphylogeny.fr for both), PhyML-SMS (https://www.atgc-montpellier.fr) for tree inference, and exported to the Interactive Tree Of Life (iTOL; https://itol.embl.de) for display and manipulation. B. pseudomallei strains were isolated in Thailand (T), Australia (A), India (I) and Papua New Guinea (P). Scale bar indicates number of substitutions per site. bimA, Burkholderia intracellular motility factor A.

Figure 1. Phylogenetic tree based on bimABp and bimABm alleles from strains of Burkholderia pseudomallei, B. mallei, and B. humptydooensis, showing location of B. mallei ATS2021 (arrow), the causative strain in an an outbreak of 4 cases, 2 of them fatal, in the United States in 2021. NGPhylogeny.fr (12) was used to build the tree in “A la Carte” mode, and it used MUSCLE for multiple alignment, Gblocks for automatic alignment curation (https://NGphylogeny.fr for both), PhyML-SMS (https://www.atgc-montpellier.fr) for tree inference, and exported to the Interactive Tree Of Life (iTOL; https://itol.embl.de) for display and manipulation. B. pseudomallei strains were isolated in Thailand (T), Australia (A), India (I) and Papua New Guinea (P). Scale bar indicates number of substitutions per site. bimA, Burkholderia intracellular motility factor A.

Main Article

References
  1. Currie  BJ. Melioidosis: evolving concepts in epidemiology, pathogenesis, and treatment. Semin Respir Crit Care Med. 2015;36:11125. DOIPubMedGoogle Scholar
  2. Currie  BJ, Meumann  EM, Kaestli  M. The expanding global footprint of Burkholderia pseudomallei and melioidosis. Am J Trop Med Hyg. 2023;108:10813. DOIPubMedGoogle Scholar
  3. Chantratita  N, Phunpang  R, Yarasai  A, Dulsuk  A, Yimthin  T, Onofrey  LA, et al. Characteristics and one year outcomes of melioidosis patients in northeastern Thailand: a prospective, multicenter cohort study. Lancet Reg Health Southeast Asia. 2023;9:9. DOIPubMedGoogle Scholar
  4. Currie  BJ, Mayo  M, Ward  LM, Kaestli  M, Meumann  EM, Webb  JR, et al. The Darwin Prospective Melioidosis Study: a 30-year prospective, observational investigation. Lancet Infect Dis. 2021;21:173746. DOIPubMedGoogle Scholar
  5. Currie  BJ, Fisher  DA, Howard  DM, Burrow  JN. Neurological melioidosis. Acta Trop. 2000;74:14551. DOIPubMedGoogle Scholar
  6. Wongwandee  M, Linasmita  P. Central nervous system melioidosis: A systematic review of individual participant data of case reports and case series. PLoS Negl Trop Dis. 2019;13:e0007320. DOIPubMedGoogle Scholar
  7. Sullivan  RP, Marshall  CS, Anstey  NM, Ward  L, Currie  BJ. 2020 Review and revision of the 2015 Darwin melioidosis treatment guideline; paradigm drift not shift. PLoS Negl Trop Dis. 2020;14:e0008659. DOIPubMedGoogle Scholar
  8. Gora  H, Hasan  T, Smith  S, Wilson  I, Mayo  M, Woerle  C, et al. Melioidosis of the central nervous system; impact of the bimABm allele on patient presentation and outcome. Clin Infect Dis. 2022;•••:ciac111.PubMedGoogle Scholar
  9. Mukhopadhyay  C, Kaestli  M, Vandana  KE, Sushma  K, Mayo  M, Richardson  L, et al. Molecular characterization of clinical Burkholderia pseudomallei isolates from India. Am J Trop Med Hyg. 2011;85:1213. DOIPubMedGoogle Scholar
  10. Limmathurotsakul  D, Dance  DA, Wuthiekanun  V, Kaestli  M, Mayo  M, Warner  J, et al. Systematic review and consensus guidelines for environmental sampling of Burkholderia pseudomallei. PLoS Negl Trop Dis. 2013;7:e2105. DOIPubMedGoogle Scholar
  11. Gee  JE, Bower  WA, Kunkel  A, Petras  J, Gettings  J, Bye  M, et al. Multistate outbreak of melioidosis associated with imported aromatherapy spray. N Engl J Med. 2022;386:8618. DOIPubMedGoogle Scholar
  12. Petras  JK, Elrod  MG, Ty  M, Adams  P, Zahner  D, Adams  A, et al. Notes from the field: Burkholderia pseudomallei detected in a raccoon carcass linked to a multistate aromatherapy-associated melioidosis outbreak—Texas, 2022. MMWR Morb Mortal Wkly Rep. 2022;71:15978. DOIPubMedGoogle Scholar
  13. Matthews  RJ, Smith  S, Wilson  I, Tjahjono  R, Young  S, Hanson  J. Case report: vagal nerve neuritis associated with pulmonary melioidosis provides potential insights into the pathophysiology of neuromelioidosis. Am J Trop Med Hyg. 2023;108:12124. DOIPubMedGoogle Scholar
  14. St John  JA, Walkden  H, Nazareth  L, Beagley  KW, Ulett  GC, Batzloff  MR, et al. Burkholderia pseudomallei rapidly infects the brain stem and spinal cord via the trigeminal nerve after intranasal inoculation. Infect Immun. 2016;84:26818. DOIPubMedGoogle Scholar
  15. Walkden  H, Delbaz  A, Nazareth  L, Batzloff  M, Shelper  T, Beacham  IR, et al. Burkholderia pseudomallei invades the olfactory nerve and bulb after epithelial injury in mice and causes the formation of multinucleated giant glial cells in vitro. PLoS Negl Trop Dis. 2020;14:e0008017. DOIPubMedGoogle Scholar
  16. St John  JA, Ekberg  JA, Dando  SJ, Meedeniya  AC, Horton  RE, Batzloff  M, et al. Burkholderia pseudomallei penetrates the brain via destruction of the olfactory and trigeminal nerves: implications for the pathogenesis of neurological melioidosis. MBio. 2014;5:e00025. DOIPubMedGoogle Scholar
  17. Burnard  D, Bauer  MJ, Falconer  C, Gassiep  I, Norton  RE, Paterson  DL, et al. Clinical Burkholderia pseudomallei isolates from north Queensland carry diverse bimABm genes that are associated with central nervous system disease and are phylogenomically distinct from other Australian strains. PLoS Negl Trop Dis. 2022;16:e0009482. DOIPubMedGoogle Scholar
  18. Sarovich  DS, Price  EP, Webb  JR, Ward  LM, Voutsinos  MY, Tuanyok  A, et al. Variable virulence factors in Burkholderia pseudomallei (melioidosis) associated with human disease. PLoS One. 2014;9:e91682. DOIPubMedGoogle Scholar
  19. Trevino  SR, Klimko  CP, Reed  MC, Aponte-Cuadrado  MJ, Hunter  M, Shoe  JL, et al. Disease progression in mice exposed to low-doses of aerosolized clinical isolates of Burkholderia pseudomallei. PLoS One. 2018;13:e0208277. DOIPubMedGoogle Scholar
  20. Guyton  AC. Measurement of the respiratory volumes of laboratory animals. Am J Physiol. 1947;150:707. DOIPubMedGoogle Scholar
  21. Marchetti  R, Dillon  MJ, Burtnick  MN, Hubbard  MA, Kenfack  MT, Blériot  Y, et al. Burkholderia pseudomallei capsular polysaccharide recognition by a monoclonal antibody reveals key details toward a biodefense vaccine and diagnostics against melioidosis. ACS Chem Biol. 2015;10:2295302. DOIPubMedGoogle Scholar
  22. Stefan  CP, Arnold  CE, Shoemaker  CJ, Zumbrun  EE, Altamura  LA, Douglas  CE, et al. Transcriptomic analysis reveals host miRNAs correlated with immune gene dysregulation during fatal disease progression in the Ebola virus cynomolgus macaque disease model. Microorganisms. 2021;9:665. DOIPubMedGoogle Scholar
  23. Perkins  JR, Dawes  JM, McMahon  SB, Bennett  DL, Orengo  C, Kohl  M. ReadqPCR and NormqPCR: R packages for the reading, quality checking and normalisation of RT-qPCR quantification cycle (Cq) data. BMC Genomics. 2012;13:296. DOIPubMedGoogle Scholar
  24. Reckseidler  SL, DeShazer  D, Sokol  PA, Woods  DE. Detection of bacterial virulence genes by subtractive hybridization: identification of capsular polysaccharide of Burkholderia pseudomallei as a major virulence determinant. Infect Immun. 2001;69:3444. DOIPubMedGoogle Scholar
  25. DeShazer  D, Brett  PJ, Woods  DE. The type II O-antigenic polysaccharide moiety of Burkholderia pseudomallei lipopolysaccharide is required for serum resistance and virulence. Mol Microbiol. 1998;30:1081100. DOIPubMedGoogle Scholar
  26. Burtnick  MN, Brett  PJ, Harding  SV, Ngugi  SA, Ribot  WJ, Chantratita  N, et al. The cluster 1 type VI secretion system is a major virulence determinant in Burkholderia pseudomallei. Infect Immun. 2011;79:151225. DOIPubMedGoogle Scholar
  27. Holden  MT, Titball  RW, Peacock  SJ, Cerdeño-Tárraga  AM, Atkins  T, Crossman  LC, et al. Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci U S A. 2004;101:142405. DOIPubMedGoogle Scholar
  28. Benanti  EL, Nguyen  CM, Welch  MD. Virulent Burkholderia species mimic host actin polymerases to drive actin-based motility. Cell. 2015;161:34860. DOIPubMedGoogle Scholar
  29. Morris  JL, Fane  A, Sarovich  DS, Price  EP, Rush  CM, Govan  BL, et al. Increased neurotropic threat from Burkholderia pseudomallei strains with a B. mallei–like variation in the bimA motility gene, Australia. Emerg Infect Dis. 2017;23:7409. DOIPubMedGoogle Scholar
  30. Sitthidet  C, Stevens  JM, Chantratita  N, Currie  BJ, Peacock  SJ, Korbsrisate  S, et al. Prevalence and sequence diversity of a factor required for actin-based motility in natural populations of Burkholderia species. J Clin Microbiol. 2008;46:241822. DOIPubMedGoogle Scholar
  31. Jayasinghearachchi  HS, Corea  EM, Jayaratne  KI, Fonseka  RA, Muthugama  TA, Masakorala  J, et al. Biogeography and genetic diversity of clinical isolates of Burkholderia pseudomallei in Sri Lanka. PLoS Negl Trop Dis. 2021;15:e0009917. DOIPubMedGoogle Scholar
  32. Janesomboon  S, Muangsombut  V, Srinon  V, Meethai  C, Tharinjaroen  CS, Amornchai  P, et al. Detection and differentiation of Burkholderia species with pathogenic potential in environmental soil samples. PLoS One. 2021;16:e0245175. DOIPubMedGoogle Scholar
  33. Welkos  SL, Klimko  CP, Kern  SJ, Bearss  JJ, Bozue  JA, Bernhards  RC, et al. Characterization of Burkholderia pseudomallei strains using a murine intraperitoneal infection model and in vitro macrophage assays. PLoS One. 2015;10:e0124667. DOIPubMedGoogle Scholar
  34. Limmathurotsakul  D, Funnell  SG, Torres  AG, Morici  LA, Brett  PJ, Dunachie  S, et al.; Steering Group on Melioidosis Vaccine Development. Consensus on the development of vaccines against naturally acquired melioidosis. Emerg Infect Dis. 2015;21:e141480. DOIPubMedGoogle Scholar
  35. Conejero  L, Patel  N, de Reynal  M, Oberdorf  S, Prior  J, Felgner  PL, et al. Low-dose exposure of C57BL/6 mice to burkholderia pseudomallei mimics chronic human melioidosis. Am J Pathol. 2011;179:27080. DOIPubMedGoogle Scholar
  36. Nelson  M, Barnes  KB, Davies  CH, Cote  CK, Meinig  JM, Biryukov  SS, et al. The BALB/c mouse model for the evaluation of therapies to treat infections with aerosolized Burkholderia pseudomallei. Antibiotics (Basel). 2023;12:506. DOIPubMedGoogle Scholar
  37. Bearss  JJ, Hunter  M, Dankmeyer  JL, Fritts  KA, Klimko  CP, Weaver  CH, et al. Characterization of pathogenesis of and immune response to Burkholderia pseudomallei K96243 using both inhalational and intraperitoneal infection models in BALB/c and C57BL/6 mice. PLoS One. 2017;12:e0172627. DOIPubMedGoogle Scholar
  38. Stassart  RM, Möbius  W, Nave  KA, Edgar  JM. The axon-myelin unit in development and degenerative disease. Front Neurosci. 2018;12:467. DOIPubMedGoogle Scholar
  39. Molina-Gonzalez  I, Miron  VE, Antel  JP. Chronic oligodendrocyte injury in central nervous system pathologies. Commun Biol. 2022;5:1274. DOIPubMedGoogle Scholar
  40. Kenigsbuch  M, Bost  P, Halevi  S, Chang  Y, Chen  S, Ma  Q, et al. A shared disease-associated oligodendrocyte signature among multiple CNS pathologies. Nat Neurosci. 2022;25:87686. DOIPubMedGoogle Scholar
  41. Graf  LM, Rosenkranz  SC, Hölzemer  A, Hagel  C, Goebell  E, Jordan  S, et al. Clinical presentation and disease course of 37 consecutive cases of progressive multifocal leukoencephalopathy (PML) at a German tertiary-care hospital: a retrospective observational study. Front Neurol. 2021;12:632535. DOIPubMedGoogle Scholar
  42. Cortese  I, Reich  DS, Nath  A. Progressive multifocal leukoencephalopathy and the spectrum of JC virus-related disease. Nat Rev Neurol. 2021;17:3751. DOIPubMedGoogle Scholar
  43. Ramesh  G, Borda  JT, Dufour  J, Kaushal  D, Ramamoorthy  R, Lackner  AA, et al. Interaction of the Lyme disease spirochete Borrelia burgdorferi with brain parenchyma elicits inflammatory mediators from glial cells as well as glial and neuronal apoptosis. Am J Pathol. 2008;173:141527. DOIPubMedGoogle Scholar
  44. Trevino  SR, Dankmeyer  JL, Fetterer  DP, Klimko  CP, Raymond  JLW, Moreau  AM, et al. Comparative virulence of three different strains of Burkholderia pseudomallei in an aerosol non-human primate model. PLoS Negl Trop Dis. 2021;15:e0009125. DOIPubMedGoogle Scholar
  45. Taweechaisupapong  S, Kaewpa  C, Arunyanart  C, Kanla  P, Homchampa  P, Sirisinha  S, et al. Virulence of Burkholderia pseudomallei does not correlate with biofilm formation. Microb Pathog. 2005;39:7785. DOIPubMedGoogle Scholar
  46. Boisvert  AA, Cheng  MP, Sheppard  DC, Nguyen  D. Microbial biofilms in pulmonary and critical care diseases. Ann Am Thorac Soc. 2016;13:161523. DOIPubMedGoogle Scholar
  47. Chakraborty  P, Bajeli  S, Kaushal  D, Radotra  BD, Kumar  A. Biofilm formation in the lung contributes to virulence and drug tolerance of Mycobacterium tuberculosis. Nat Commun. 2021;12:1606. DOIPubMedGoogle Scholar
  48. Nyanasegran  PK, Nathan  S, Firdaus-Raih  M, Muhammad  NAN, Ng  CL. Biofilm signaling, composition and regulation in Burkholderia pseudomallei. J Microbiol Biotechnol. 2023;33:1527. DOIPubMedGoogle Scholar
  49. Petras  JK, Elrod  MG, Ty  MC, Dawson  P, O’Laughlin  K, Gee  JE, et al. Locally acquired melioidosis linked to environment—Mississippi, 2020–2023. N Engl J Med. 2023;389:235562. DOIPubMedGoogle Scholar

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