The Rapid Emergence of Hypervirulent Klebsiella Species and Burkholderia pseudomallei as Major Health Threats in Southeast Asia: The Urgent Need for Recognition as Neglected Tropical Diseases
Abstract
:1. Introduction
2. Melioidosis
2.1. Introduction
2.2. Epidemiology
2.3. Clinical Syndrome
2.4. Diagnosis
2.5. Treatment
2.6. Challenges
3. Hypervirulent Klebsiella pneumoniae
3.1. Introduction
3.2. Epidemiology
3.3. Clinical Syndrome
3.4. Diagnosis
3.5. Treatment
3.6. Challenges
4. Strategy
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- World Health Organization. Ending the Neglect to Attain the Sustainable Development Goals: A Road Map for Neglected Tropical Diseases 2021–2030; World Health Organization: Geneva, Switzerland, 2020. [Google Scholar]
- Hotez, P.J.; Aksoy, S.; Brindley, P.J.; Kamhawi, S. What Constitutes a Neglected Tropical Disease? PLoS Negl. Trop. Dis. 2020, 14, e0008001. [Google Scholar] [CrossRef] [PubMed]
- Limmathurotsakul, D.; Golding, N.; Dance, D.A.B.; Messina, J.P.; Pigott, D.M.; Moyes, C.L.; Rolim, D.B.; Bertherat, E.; Day, N.P.J.; Peacock, S.J.; et al. Predicted Global Distribution of Burkholderia Pseudomallei and Burden of Melioidosis. Nat. Microbiol. 2016, 1, 15008. [Google Scholar] [CrossRef] [PubMed]
- Fang, C.T.; Chuang, Y.P.; Shun, C.T.; Chang, S.C.; Wang, J.T. A Novel Virulence Gene in Klebsiella pneumoniae Strains Causing Primary Liver Abscess and Septic Metastatic Complications. J. Exp. Med. 2004, 199, 697–705. [Google Scholar] [CrossRef] [PubMed]
- Shankar, C.; Nabarro, L.E.; Anandan, S.; Ravi, R.; Babu, P.; Munusamy, E.; Jeyaseelan, V.; Rupali, P.; Verghese, V.P.; Veeraraghavan, B. Extremely High Mortality Rates in Patients with Carbapenem-Resistant, Hypermucoviscous Klebsiella pneumoniae Blood Stream Infections. J. Assoc. Physicians India 2018, 66, 13–16. [Google Scholar] [PubMed]
- Wuthiekanun, V.; Cheng, A.C.; Chierakul, W.; Amornchai, P.; Limmathurotsakul, D.; Chaowagul, W.; Simpson, A.J.H.; Short, J.M.; Wongsuvan, G.; Maharjan, B.; et al. Trimethoprim/Sulfamethoxazole Resistance in Clinical Isolates of Burkholderia pseudomallei. J. Antimicrob. Chemother. 2005, 55, 1029–1031. [Google Scholar] [CrossRef] [PubMed]
- Wiersinga, W.J.; Virk, H.S.; Torres, A.G.; Currie, B.J.; Peacock, S.J.; Dance, D.A.B.; Limmathurotsakul, D. Melioidosis. Nat. Rev. Dis. Primers 2018, 4, 17107. [Google Scholar] [CrossRef] [PubMed]
- Meumann, E.M.; Limmathurotsakul, D.; Dunachie, S.J.; Wiersinga, W.J.; Currie, B.J. Burkholderia pseudomallei and Melioidosis. Nat. Rev. Microbiol. 2023, 22, 155–169. [Google Scholar] [CrossRef] [PubMed]
- Selvam, K.; Ganapathy, T.; Najib, M.A.; Khalid, M.F.; Abdullah, N.A.; Harun, A.; Wan Mohammad, W.M.Z.; Aziah, I. Burden and Risk Factors of Melioidosis in Southeast Asia: A Scoping Review. Int. J. Environ. Res. Public Health 2022, 19, 15475. [Google Scholar] [CrossRef] [PubMed]
- Jatapai, A.; Gregory, C.J.; Thamthitiwat, S.; Tanwisaid, K.; Bhengsri, S.; Baggett, H.C.; Sangwichian, O.; Jorakate, P.; MacArthur, J.R. Hospitalized Bacteremic Melioidosis in Rural Thailand: 2009–2013. Am. J. Trop. Med. Hyg. 2018, 98, 1585. [Google Scholar] [CrossRef] [PubMed]
- Stoesser, N.; Pocock, J.; Moore, C.E.; Soeng, S.; Chhat, H.P.; Sar, P.; Limmathurotsakul, D.; Day, N.; Thy, V.; Sar, V.; et al. Pediatric Suppurative Parotitis in Cambodia between 2007 and 2011. Pediatr. Infect. Dis. J. 2012, 31, 865–868. [Google Scholar] [CrossRef] [PubMed]
- Win, M.M.; Win, K.K.N.; Wah, T.T.; Aye, S.N.; Htwe, T.T.; Zin, K.N.; Aung, M.T.; Aung, W.W.; Ashley, E.A.; Smithuis, F.; et al. Enhanced Melioidosis Surveillance in Patients Attending Four Tertiary Hospitals in Yangon, Myanmar. Epidemiol. Infect. 2021, 149, 1–23. [Google Scholar] [CrossRef] [PubMed]
- Gassiep, I.; Armstrong, M.; Norton, R. Human Melioidosis. Clin. Microbiol. Rev. 2020, 33, e00006-19. [Google Scholar] [CrossRef] [PubMed]
- Mohapatra, P.R.; Mishra, B. Burden of Melioidosis in India and South Asia: Challenges and Ways Forward. Lancet Reg. Health Southeast. Asia 2022, 2, 100004. [Google Scholar] [CrossRef] [PubMed]
- Suntornsut, P.; Wongsuwan, N.; Malasit, M.; Kitphati, R.; Michie, S.; Peacock, S.J.; Limmathurotsakul, D. Barriers and Recommended Interventions to Prevent Melioidosis in Northeast Thailand: A Focus Group Study Using the Behaviour Change Wheel. PLoS Negl. Trop. Dis. 2016, 10, e0004823. [Google Scholar] [CrossRef] [PubMed]
- Tan, K.S.; Lee, K.O.; Low, K.C.; Gamage, A.M.; Liu, Y.; Tan, G.Y.G.; Koh, H.Q.V.; Alonso, S.; Gan, Y.H. Glutathione Deficiency in Type 2 Diabetes Impairs Cytokine Responses and Control of Intracellular Bacteria. J. Clin. Investig. 2012, 122, 2289. [Google Scholar] [CrossRef]
- Morris, J.L.; Govan, B.L.; Rush, C.M.; Ketheesan, N. Identification of Defective Early Immune Responses to Burkholderia Pseudomallei Infection in a Diet-Induced Murine Model of Type 2 Diabetes. Microbes Infect. 2021, 23, 104793. [Google Scholar] [CrossRef] [PubMed]
- Hussin, A.; Nor Rahim, M.Y.; Dalusim, F.; Shahidan, M.A.; Nathan, S.; Ibrahim, N. Improving the Clinical Recognition, Prognosis, and Treatment of Melioidosis through Epidemiology and Clinical Findings: The Sabah Perspective. PLoS Negl. Trop. Dis. 2023, 17, e0011696. [Google Scholar] [CrossRef] [PubMed]
- Churuangsuk, C.; Chusri, S.; Hortiwakul, T.; Charernmak, B.; Silpapojakul, K. Characteristics, Clinical Outcomes and Factors Influencing Mortality of Patients with Melioidosis in Southern Thailand: A 10-Year Retrospective Study. Asian Pac. J. Trop. Med. 2016, 9, 256–260. [Google Scholar] [CrossRef] [PubMed]
- Dance, D.A.B.; Limmathurotsakul, D. Global Burden and Challenges of Melioidosis. Trop. Med. Infect. Dis. 2018, 3, 13. [Google Scholar] [CrossRef] [PubMed]
- Smith, S.; Hanson, J.; Currie, B.J. Melioidosis: An Australian Perspective. Trop. Med. Infect. Dis. 2018, 3, 27. [Google Scholar] [CrossRef]
- Hayden, H.S.; Lim, R.; Brittnacher, M.J.; Sims, E.H.; Ramage, E.R.; Fong, C.; Wu, Z.; Crist, E.; Chang, J.; Zhou, Y.; et al. Evolution of Burkholderia Pseudomallei in Recurrent Melioidosis. PLoS ONE 2012, 7, e36507. [Google Scholar] [CrossRef] [PubMed]
- Chantratita, N.; Phunpang, R.; Yarasai, A.; Dulsuk, A.; Yimthin, T.; Onofrey, L.A.; Coston, T.D.; Thiansukhon, E.; Chaisuksant, S.; Tanwisaid, K.; 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, 100118. [Google Scholar] [CrossRef] [PubMed]
- Chakravorty, A.; Heath, C.H. Melioidosis: An Updated Review. Aust. J. Gen. Pract. 2019, 48, 327–332. [Google Scholar] [CrossRef] [PubMed]
- Public Health England. Identification of Pseudomonas Species and Other Non Glucose Fermenters. In UK Standards for Microbiology Investigations; Public Health England: London, UK, 2015. [Google Scholar]
- Zueter, A.R.; Yean, C.Y.; Abumarzouq, M.; Rahman, Z.A.; Deris, Z.Z.; Harun, A. The Epidemiology and Clinical Spectrum of Melioidosis in a Teaching Hospital in a North-Eastern State of Malaysia: A Fifteen-Year Review. BMC Infect. Dis. 2016, 16, 333. [Google Scholar] [CrossRef] [PubMed]
- Burkholderia Pseudomallei Calibration of Zone Diameter Breakpoints to MIC Values. Available online: https://www.eucast.org/eucast_news/news_singleview?tx_ttnews%5Btt_news%5D=390&cHash=92ef60baaab9a71ed77e722f4b1a7766 (accessed on 7 April 2024).
- Wayne, P. M45 Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria, 3rd ed.; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2015. [Google Scholar]
- Suttisunhakul, V.; Pumpuang, A.; Ekchariyawat, P.; Wuthiekanun, V.; Elrod, M.G.; Turner, P.; Currie, B.J.; Phetsouvanh, R.; Dance, D.A.B.; Limmathurotsakul, D.; et al. Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry for the Identification of Burkholderia pseudomallei from Asia and Australia and Differentiation between Burkholderia Species. PLoS ONE 2017, 12, e0175294. [Google Scholar] [CrossRef] [PubMed]
- Health and Safety Executive. The Approved List of Biological Agents: Advisory Committee on Dangerous Pathogens; Health and Safety Executive: Bootle, UK, 2023. [Google Scholar]
- Woods, K.L.; Boutthasavong, L.; NicFhogartaigh, C.; Lee, S.J.; Davong, V.; AuCoin, D.P.; Dancea, D.A.B. Evaluation of a Rapid Diagnostic Test for Detection of Burkholderia pseudomallei in the Lao People’s Democratic Republic. J. Clin. Microbiol. 2018, 56, e02002-17. [Google Scholar] [CrossRef] [PubMed]
- Currie, B.J.; Woerle, C.; Mayo, M.; Meumann, E.M.; Baird, R.W. What Is the Role of Lateral Flow Immunoassay for the Diagnosis of Melioidosis? Open Forum Infect. Dis. 2022, 9, ofac149. [Google Scholar] [CrossRef] [PubMed]
- Hoffmaster, A.R.; Aucoin, D.; Baccam, P.; Baggett, H.C.; Baird, R.; Bhengsri, S.; Blaney, D.D.; Brett, P.J.; Brooks, T.J.G.; Brown, K.A.; et al. Melioidosis Diagnostic Workshop, 2013. Emerg. Infect. Dis. 2015, 21, e141045. [Google Scholar] [CrossRef] [PubMed]
- Sullivan, R.P.; Marshall, C.S.; Anstey, N.M.; Ward, L.; Currie, B.J. 2020 Review and Revision of the 2015 Darwin Melioidosis Treatment Guideline; Paradigm Drift Not Shift. PLoS Neglected Trop. Dis. 2020, 14, e0008659. [Google Scholar] [CrossRef] [PubMed]
- Pitman, M.C.; Luck, T.; Marshall, C.S.; Anstey, N.M.; Ward, L.; Currie, B.J. Intravenous Therapy Duration and Outcomes in Melioidosis: A New Treatment Paradigm. PLoS Neglected Trop. Dis. 2015, 9, e0003586. [Google Scholar] [CrossRef] [PubMed]
- Currie, B.J.; Mayo, M.; Ward, L.M.; Kaestli, M.; Meumann, E.M.; Webb, J.R.; Woerle, C.; Baird, R.W.; Price, R.N.; Marshall, C.S.; et al. The Darwin Prospective Melioidosis Study: A 30-Year Prospective, Observational Investigation. Lancet Infect. Dis. 2021, 21, 1737–1746. [Google Scholar] [CrossRef]
- Inglis, T.J.J.; Rodrigues, F.; Rigby, P.; Norton, R.; Currie, B.J. Comparison of the Susceptibilities of Burkholderia Pseudomallei to Meropenem and Ceftazidime by Conventional and Intracellular Methods. Antimicrob. Agents Chemother. 2004, 48, 2999–3005. [Google Scholar] [CrossRef] [PubMed]
- Wuthiekanun, V.; Amornchai, P.; Saiprom, N.; Chantratita, N.; Chierakul, W.; Koh, G.C.K.W.; Chaowagul, W.; Day, N.P.J.; Limmathurotsakul, D.; Peacock, S.J. Survey of Antimicrobial Resistance in Clinical Burkholderia Pseudomallei Isolates over Two Decades in Northeast Thailand. Antimicrob. Agents Chemother. 2011, 55, 5388–5391. [Google Scholar] [CrossRef] [PubMed]
- Dance, D.A.B.; Davong, V.; Soeng, S.; Phetsouvanh, R.; Newton, P.N.; Turner, P. Trimethoprim/Sulfamethoxazole Resistance in Burkholderia Pseudomallei. Int. J. Antimicrob. Agents 2014, 44, 368–369. [Google Scholar] [CrossRef] [PubMed]
- Hall, C.M.; Somprasong, N.; Hagen, J.P.; Nottingham, R.; Sahl, J.W.; Webb, J.R.; Mayo, M.; Currie, B.J.; Podin, Y.; Wagner, D.M.; et al. Exploring Cefiderocol Resistance Mechanisms in Burkholderia Pseudomallei. Antimicrob. Agents Chemother. 2023, 67, e0017123. [Google Scholar] [CrossRef]
- Cheng, A.C.; Limmathurotsakul, D.; Chierakul, W.; Getchalarat, N.; Wuthiekanun, V.; Stephens, D.P.; Day, N.P.J.; White, N.J.; Chaowagul, W.; Currie, B.J.; et al. A Randomized Controlled Trial of Granulocyte Colony-Stimulating Factor for the Treatment of Severe Sepsis Due to Melioidosis in Thailand. Clin. Infect. Dis. 2007, 45, 308–314. [Google Scholar] [CrossRef] [PubMed]
- Cheng, A.C.; Stephens, D.P.; Anstey, N.M.; Currie, B.J. Adjunctive Granulocyte Colony-Stimulating Factor for Treatment of Septic Shock Due to Melioidosis. Clin. Infect. Dis. 2004, 38, 32–37. [Google Scholar] [CrossRef] [PubMed]
- Wuthiekanun, V.; Chierakul, W.; Rattanalertnavee, J.; Langa, S.; Sirodom, D.; Wattanawaitunechai, C.; Winothai, W.; White, N.J.; Day, N.; Peacock, S.J. Serological Evidence for Increased Human Exposure to Burkholderia Pseudomallei Following the Tsunami in Southern Thailand. J. Clin. Microbiol. 2006, 44, 239. [Google Scholar] [CrossRef] [PubMed]
- Centers for Disease Control and Prevention Bioterrorism: Melioidosis. Available online: https://www.cdc.gov/melioidosis/bioterrorism/index.html (accessed on 26 January 2024).
- Dai, P.; Hu, D. The Making of Hypervirulent Klebsiella pneumoniae. J. Clin. Lab. Anal. 2022, 36, e24743. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.C.; Cheng, D.L.; Lin, C.L. Klebsiella pneumoniae Liver Abscess Associated with Septic Endophthalmitis. Arch. Intern. Med. 1986, 146, 1913–1916. [Google Scholar] [CrossRef] [PubMed]
- Fodah, R.A.; Scott, J.B.; Tam, H.H.; Yan, P.; Pfeffer, T.L.; Bundschuh, R.; Warawa, J.M. Correlation of Klebsiella pneumoniae Comparative Genetic Analyses with Virulence Profiles in a Murine Respiratory Disease Model. PLoS ONE 2014, 9, e107394. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.T.; Der Wang, F.; Wu, P.F.; Fung, C.P. Klebsiella pneumoniae Liver Abscess in Diabetic Patients: Association of Glycemic Control with the Clinical Characteristics. BMC Infect. Dis. 2013, 13, 56. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.; Guo, J. Hypervirulent Klebsiella pneumoniae (Hypermucoviscous and Aerobactin Positive) Infection over 6 Years in the Elderly in China: Antimicrobial Resistance Patterns, Molecular Epidemiology and Risk Factor. Ann. Clin. Microbiol. Antimicrob. 2019, 18, 4. [Google Scholar] [CrossRef] [PubMed]
- Lee, I.R.; Sng, E.; Lee, K.O.; Molton, J.S.; Chan, M.; Kalimuddin, S.; Izharuddin, E.; Lye, D.C.; Archuleta, S.; Gan, Y.H. Comparison of Diabetic and Non-Diabetic Human Leukocytic Responses to Different Capsule Types of Klebsiella pneumoniae Responsible for Causing Pyogenic Liver Abscess. Front. Cell Infect. Microbiol. 2017, 7, 275758. [Google Scholar] [CrossRef] [PubMed]
- Yu, V.L.; Hansen, D.S.; Wen, C.K.; Sagnimeni, A.; Klugman, K.P.; Von Gottberg, A.; Goossens, H.; Wagener, M.M.; Benedi, V.J.; Casellas, J.M.; et al. Virulence Characteristics of Klebsiella and Clinical Manifestations of K. pneumoniae Bloodstream Infections. Emerg. Infect. Dis. 2007, 13, 986–993. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Zhang, H.; Liao, X. Hypervirulent Klebsiella pneumoniae. Infect. Drug Resist. 2023, 16, 5243–5249. [Google Scholar] [CrossRef] [PubMed]
- Dong, N.; Yang, X.; Chan, E.W.C.; Zhang, R.; Chen, S. Klebsiella Species: Taxonomy, Hypervirulence and Multidrug Resistance. EBioMedicine 2022, 79, 103998. [Google Scholar] [CrossRef] [PubMed]
- Wu, K.M.; Li, N.H.; Yan, J.J.; Tsao, N.; Liao, T.L.; Tsai, H.C.; Fung, C.P.; Chen, H.J.; Liu, Y.M.; Wang, J.T.; et al. Genome Sequencing and Comparative Analysis of Klebsiella pneumoniae NTUH-K2044, a Strain Causing Liver Abscess and Meningitis. J. Bacteriol. 2009, 191, 4492–4501. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.T.; Chang, H.Y.; Lai, Y.C.; Pan, C.C.; Tsai, S.F.; Peng, H.L. Sequencing and Analysis of the Large Virulence Plasmid PLVPK of Klebsiella pneumoniae CG43. Gene 2004, 337, 189–198. [Google Scholar] [CrossRef]
- Yang, X.; Sun, Q.; Li, J.; Jiang, Y.; Li, Y.; Lin, J.; Chen, K.; Chan, E.W.C.; Zhang, R.; Chen, S. Molecular Epidemiology of Carbapenem-Resistant Hypervirulent Klebsiella pneumoniae in China. Emerg. Microbes Infect. 2022, 11, 841–849. [Google Scholar] [CrossRef] [PubMed]
- Cortés, G.; Borrell, N.; De Astorza, B.; Gómez, C.; Sauleda, J.; Albertí, S. Molecular Analysis of the Contribution of the Capsular Polysaccharide and the Lipopolysaccharide O Side Chain to the Virulence of Klebsiella pneumoniae in a Murine Model of Pneumonia. Infect. Immun. 2002, 70, 2583–2590. [Google Scholar] [CrossRef] [PubMed]
- Lai, Y.C.; Peng, H.L.; Chang, H.Y. RmpA2, an Activator of Capsule Biosynthesis in Klebsiella pneumoniae CG43, Regulates K2 Cps Gene Expression at the Transcriptional Level. J. Bacteriol. 2003, 185, 788–800. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Shen, D.; Wu, H.; Ma, Y. Resistance of Hypervirulent Klebsiella pneumoniae to Both Intracellular and Extracellular Killing of Neutrophils. PLoS ONE 2017, 12, e0173638. [Google Scholar] [CrossRef] [PubMed]
- Drakesmith, H.; Prentice, A.M. Hepcidin and the Iron-Infection Axis. Science 2012, 338, 768–772. [Google Scholar] [CrossRef] [PubMed]
- Russo, T.A.; Olson, R.; MacDonald, U.; Beanan, J.; Davidsona, B.A. Aerobactin, but Not Yersiniabactin, Salmochelin, or Enterobactin, Enables the Growth/Survival of Hypervirulent (Hypermucoviscous) Klebsiella pneumoniae Ex Vivo and in Vivo. Infect. Immun. 2015, 83, 3325–3333. [Google Scholar] [CrossRef] [PubMed]
- Russo, T.A.; Olson, R.; Fang, C.T.; Stoesser, N.; Miller, M.; MacDonald, U.; Hutson, A.; Barker, J.H.; La Hoz, R.M.; Johnson, J.R.; et al. Identification of Biomarkers for Differentiation of Hypervirulent Klebsiella pneumoniae from Classical K. pneumoniae. J. Clin. Microbiol. 2018, 56, 776–794. [Google Scholar] [CrossRef] [PubMed]
- Fazili, T.; Sharngoe, C.; Endy, T.; Kiska, D.; Javaid, W.; Polhemus, M. Klebsiella pneumoniae Liver Abscess: An Emerging Disease. Am. J. Med. Sci. 2016, 351, 297–304. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.R.; Lee, J.H.; Park, K.S.; Jeon, J.H.; Kim, Y.B.; Cha, C.J.; Jeong, B.C.; Lee, S.H. Antimicrobial Resistance of Hypervirulent Klebsiella pneumoniae: Epidemiology, Hypervirulence-Associated Determinants, and Resistance Mechanisms. Front. Cell Infect. Microbiol. 2017, 7, 483. [Google Scholar] [CrossRef] [PubMed]
- Lee, I.R.; Molton, J.S.; Wyres, K.L.; Gorrie, C.; Wong, J.; Hoh, C.H.; Teo, J.; Kalimuddin, S.; Lye, D.C.; Archuleta, S.; et al. Differential Host Susceptibility and Bacterial Virulence Factors Driving Klebsiella Liver Abscess in an Ethnically Diverse Population. Sci. Rep. 2016, 6, 29316. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.T.; Siu, L.K.; Lin, J.C.; Chen, T.L.; Tseng, C.P.; Yeh, K.M.; Chang, F.Y.; Fung, C.P. Seroepidemiology of Klebsiella pneumoniae Colonizing the Intestinal Tract of Healthy Chinese and Overseas Chinese Adults in Asian Countries. BMC Microbiol. 2012, 12, 13. [Google Scholar] [CrossRef] [PubMed]
- Harada, S.; Tateda, K.; Mitsui, H.; Hattori, Y.; Okubo, M.; Kimura, S.; Sekigawa, K.; Kobayashi, K.; Hashimoto, N.; Itoyama, S.; et al. Familial Spread of a Virulent Clone of Klebsiella pneumoniae Causing Primary Liver Abscess. J. Clin. Microbiol. 2011, 49, 2354–2356. [Google Scholar] [CrossRef] [PubMed]
- Kong, Z.X.; Karunakaran, R.; Abdul Jabar, K.; Ponnampalavanar, S.; Chong, C.W.; Teh, C.S.J. The Detection of Hypermucoviscous Carbapenem-Resistant Klebsiella pneumoniae from a Tertiary Teaching Hospital in Malaysia and Assessment of Hypermucoviscous as Marker of Hypervirulence. Microb. Drug Resist. 2021, 27, 1319–1327. [Google Scholar] [CrossRef]
- En, E.T.S.; Ismail, N.; Nasir, N.S.M.; Ismadi, Y.K.M.; Zuraina, N.M.N.N.; Hassan, S.A. Pediatric Brain Abscess with Fatal Outcome Caused by Hypervirulent Klebsiella pneumoniae, Serotype K2-ST65. J. Infect. Public Health 2023, 16, 1089–1092. [Google Scholar] [CrossRef] [PubMed]
- Nakamura, K.; Nomoto, H.; Harada, S.; Suzuki, M.; Yomono, K.; Yokochi, R.; Hagino, N.; Nakamoto, T.; Moriyama, Y.; Yamamoto, K.; et al. Infection with Capsular Genotype K1-ST23 Hypervirulent Klebsiella pneumoniae Isolates in Japan after a Stay in East Asia: Two Cases and a Literature Review. J. Infect. Chemother. 2021, 27, 1508–1512. [Google Scholar] [CrossRef] [PubMed]
- Lin, J.C.; Koh, T.H.; Lee, N.; Fung, C.P.; Chang, F.Y.; Tsai, Y.K.; Ip, M.; Siu, L.K. Genotypes and Virulence in Serotype K2 Klebsiella pneumoniae from Liver Abscess and Non-Infectious Carriers in Hong Kong, Singapore and Taiwan. Gut Pathog. 2014, 6, 21. [Google Scholar] [CrossRef]
- Spadar, A.; Perdigão, J.; Campino, S.; Clark, T.G. Large-Scale Genomic Analysis of Global Klebsiella pneumoniae Plasmids Reveals Multiple Simultaneous Clusters of Carbapenem-Resistant Hypervirulent Strains. Genome Med. 2023, 15, 3. [Google Scholar] [CrossRef] [PubMed]
- Wyres, K.L.; Nguyen, T.N.T.; Lam, M.M.C.; Judd, L.M.; Van Vinh Chau, N.; Dance, D.A.B.; Ip, M.; Karkey, A.; Ling, C.L.; Miliya, T.; et al. Genomic Surveillance for Hypervirulence and Multi-Drug Resistance in Invasive Klebsiella pneumoniae from South and Southeast Asia. Genome Med. 2020, 12, 11. [Google Scholar] [CrossRef]
- Lam, M.M.C.; Wyres, K.L.; Judd, L.M.; Wick, R.R.; Jenney, A.; Brisse, S.; Holt, K.E. Tracking Key Virulence Loci Encoding Aerobactin and Salmochelin Siderophore Synthesis in Klebsiella pneumoniae. Genome Med. 2018, 10, 77. [Google Scholar] [CrossRef] [PubMed]
- Singh, S.R.; Teo, A.K.J.; Prem, K.; Ong, R.T.H.; Ashley, E.A.; van Doorn, H.R.; Limmathurotsakul, D.; Turner, P.; Hsu, L.Y. Epidemiology of Extended-Spectrum Beta-Lactamase and Carbapenemase-Producing Enterobacterales in the Greater Mekong Subregion: A Systematic-Review and Meta-Analysis of Risk Factors Associated with Extended-Spectrum Beta-Lactamase and Carbapenemase Isolation. Front. Microbiol. 2021, 12, 695027. [Google Scholar] [CrossRef]
- Tsai, F.C.; Huang, Y.T.; Chang, L.Y.; Wang, J.T. Pyogenic Liver Abscess as Endemic Disease, Taiwan. Emerg. Infect. Dis. 2008, 14, 1592–1600. [Google Scholar] [CrossRef] [PubMed]
- Chung, D.R.; Lee, S.S.; Lee, H.R.; Kim, H.B.; Choi, H.J.; Eom, J.S.; Kim, J.S.; Choi, Y.H.; Lee, J.S.; Chung, M.H.; et al. Emerging Invasive Liver Abscess Caused by K1 Serotype Klebsiella pneumoniae in Korea. J. Infect. 2007, 54, 578–583. [Google Scholar] [CrossRef]
- Lo, J.Z.W.; Leow, J.J.J.; Ng, P.L.F.; Lee, H.Q.; Mohd Noor, N.A.; Low, J.K.; Junnarkar, S.P.; Woon, W.W.L. Predictors of Therapy Failure in a Series of 741 Adult Pyogenic Liver Abscesses. J. Hepatobiliary Pancreat. Sci. 2015, 22, 156–165. [Google Scholar] [CrossRef] [PubMed]
- Aslam, B.; Siddique, M.H.; Siddique, A.B.; Shafique, M.; Muzammil, S.; Khurshid, M.; Rasool, M.H.; Ahmad, M.; Chaudhry, T.H.; Amir, A.; et al. Distribution of Mcr-1 Harboring Hypervirulent Klebsiella pneumoniae in Clinical Specimens and Lytic Activity of Bacteriophage KpnM Against Isolates. Infect. Drug Resist. 2022, 15, 5795. [Google Scholar] [CrossRef]
- Shankar, C.; Veeraraghavan, B.; Nabarro, L.E.B.; Ravi, R.; Ragupathi, N.K.D.; Rupali, P. Whole Genome Analysis of Hypervirulent Klebsiella pneumoniae Isolates from Community and Hospital Acquired Bloodstream Infection. BMC Microbiol. 2018, 18, 6. [Google Scholar] [CrossRef] [PubMed]
- Zamani, A.; Mashouf, R.Y.; Namvar, A.M.E.; Alikhani, M.Y. Detection of MagA Gene in Klebsiella Spp. Isolated from Clinical Samples Detection of MagA. Iran. J. Basic. Med. Sci. 2013, 16, 173. [Google Scholar] [PubMed]
- Rossi, B.; Gasperini, M.L.; Leflon-Guibout, V.; Gioanni, A.; de Lastours, V.; Rossi, G.; Dokmak, S.; Ronot, M.; Roux, O.; Nicolas-Chanoine, M.H.; et al. Hypervirulent Klebsiella pneumoniaein Cryptogenic Liver Abscesses, Paris, France. Emerg. Infect. Dis. 2018, 24, 221–229. [Google Scholar] [CrossRef] [PubMed]
- Surgers, L.; Boyd, A.; Girard, P.M.; Arlet, G.; Decré, D. ESBL-Producing Strain of Hypervirulent Klebsiella pneumoniae K2, France. Emerg. Infect. Dis. 2016, 22, 1687. [Google Scholar] [CrossRef]
- Rafat, C.; Messika, J.; Barnaud, G.; Dufour, N.; Magdoud, F.; Billard-Pomarès, T.; Gaudry, S.; Dreyfuss, D.; Branger, C.; Decré, D.; et al. Hypervirulent Klebsiella pneumoniae, a 5-Year Study in a French ICU. J. Med. Microbiol. 2018, 67, 1083–1089. [Google Scholar] [CrossRef] [PubMed]
- Piazza, A.; Perini, M.; Mauri, C.; Comandatore, F.; Meroni, E.; Luzzaro, F.; Principe, L. Antimicrobial Susceptibility, Virulence, and Genomic Features of a Hypervirulent Serotype K2, ST65 Klebsiella pneumoniae Causing Meningitis in Italy. Antibiotics 2022, 11, 261. [Google Scholar] [CrossRef] [PubMed]
- Cubero, M.; Grau, I.; Tubau, F.; Pallarés, R.; Dominguez, M.A.; Liñares, J.; Ardanuy, C. Hypervirulent Klebsiella pneumoniae Clones Causing Bacteraemia in Adults in a Teaching Hospital in Barcelona, Spain (2007–2013). Clin. Microbiol. Infect. 2016, 22, 154–160. [Google Scholar] [CrossRef]
- Gundestrup, S.; Struve, C.; Stahlhut, S.G.; Hansen, D.S. First Case of Liver Abscess in Scandinavia Due to the International Hypervirulent Klebsiella pneumoniae Clone ST23. Open Microbiol. J. 2014, 8, 22. [Google Scholar] [CrossRef] [PubMed]
- Struve, C.; Roe, C.C.; Stegger, M.; Stahlhut, S.G.; Hansen, D.S.; Engelthaler, D.M.; Andersen, P.S.; Driebe, E.M.; Keim, P.; Krogfelt, K.A. Mapping the Evolution of Hypervirulent Klebsiella pneumoniae. mBio 2015, 6, e00630-15. [Google Scholar] [CrossRef] [PubMed]
- Parrott, A.M.; Shi, J.; Aaron, J.; Green, D.A.; Whittier, S.; Wu, F. Detection of Multiple Hypervirulent Klebsiella pneumoniae Strains in a New York City Hospital through Screening of Virulence Genes. Clin. Microbiol. Infect. 2021, 27, 583–589. [Google Scholar] [CrossRef] [PubMed]
- Lederman, E.R.; Crum, N.F. Pyogenic Liver Abscess with a Focus on Klebsiella pneumoniae as a Primary Pathogen: An Emerging Disease with Unique Clinical Characteristics. Am. J. Gastroenterol. 2005, 100, 322–331. [Google Scholar] [CrossRef] [PubMed]
- Coutinho, R.L.; Visconde, M.F.; Descio, F.J.; Nicoletti, A.G.; Pinto, F.C.L.; da Silva, A.C.R.; Rodrigues-Costa, F.; Gales, A.C.; Furtado, G.H.C. Community-Acquired Invasive Liver Abscess Syndrome Caused by a K1 Serotype Klebsiella pneumoniae Isolate in Brazil: A Case Report of Hypervirulent ST23. Mem. Inst. Oswaldo Cruz 2014, 109, 973–974. [Google Scholar] [CrossRef] [PubMed]
- Martin, R.M.; Cao, J.; Brisse, S.; Passet, V.; Wu, W.; Zhao, L.; Malani, P.N.; Rao, K.; Bachman, M.A. Molecular Epidemiology of Colonizing and Infecting Isolates of Klebsiella pneumoniae. mSphere 2016, 1, 261–277. [Google Scholar] [CrossRef] [PubMed]
- Russo, T.A.; Marr, C.M. Hypervirulent Klebsiella pneumoniae. Clin. Microbiol. Rev. 2019, 32, e00001-19. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.T.; Liu, C.J.; Yeh, Y.C.; Chen, T.J.; Fung, C.P. Ampicillin and Amoxicillin Use and the Risk of Klebsiella pneumoniae Liver Abscess in Taiwan. J. Infect. Dis. 2013, 208, 211–217. [Google Scholar] [CrossRef]
- Lee, H.C.; Chuang, Y.C.; Yu, W.L.; Lee, N.Y.; Chang, C.M.; Ko, N.Y.; Wang, L.R.; Ko, W.C. Clinical Implications of Hypermucoviscosity Phenotype in Klebsiella pneumoniae Isolates: Association with Invasive Syndrome in Patients with Community-Acquired Bacteraemia. J. Intern. Med. 2006, 259, 606–614. [Google Scholar] [CrossRef]
- Wu, H.; Li, D.; Zhou, H.; Sun, Y.; Guo, L.; Shen, D. Bacteremia and Other Body Site Infection Caused by Hypervirulent and Classic Klebsiella pneumoniae. Microb. Pathog. 2017, 104, 254–262. [Google Scholar] [CrossRef]
- Wang, J.H.; Liu, Y.C.; Lee, S.S.J.; Yen, M.Y.; Chen, Y.S.; Wang, J.H.; Wann, S.R.; Lin, H.H. Primary Liver Abscess Due to Klebsiella pneumoniae in Taiwan. Clin. Infect. Dis. 1998, 26, 1434–1438. [Google Scholar] [CrossRef] [PubMed]
- Yang, C.S.; Tsai, H.Y.; Sung, C.S.; Lin, K.H.; Lee, F.L.; Hsu, W.M. Endogenous Klebsiella Endophthalmitis Associated with Pyogenic Liver Abscess. Ophthalmology 2007, 114, 876–880.e2. [Google Scholar] [CrossRef] [PubMed]
- McLaughlin, M.M.; Advincula, M.R.; Malczynski, M.; Barajas, G.; Qi, C.; Scheetz, M.H. Quantifying the Clinical Virulence of Klebsiella pneumoniae Producing Carbapenemase Klebsiella pneumoniae with a Galleria Mellonella Model and a Pilot Study to Translate to Patient Outcomes. BMC Infect. Dis. 2014, 14, 31. [Google Scholar] [CrossRef] [PubMed]
- Russo, T.A.; MacDonald, U. The Galleria mellonella Infection Model Does Not Accurately Differentiate between Hypervirulent and Classical Klebsiella pneumoniae. mSphere 2020, 5, e00850-19. [Google Scholar] [CrossRef] [PubMed]
- Catalán-Nájera, J.C.; Garza-Ramos, U.; Barrios-Camacho, H. Hypervirulence and Hypermucoviscosity: Two Different but Complementary Klebsiella Spp. Phenotypes? Virulence 2017, 8, 1111–1123. [Google Scholar] [CrossRef] [PubMed]
- Yu, F.; Lv, J.; Niu, S.; Du, H.; Tang, Y.W.; Pitout, J.D.D.; Bonomo, R.A.; Kreiswirth, B.N.; Chen, L. Multiplex PCR Analysis for Rapid Detection of Klebsiella pneumoniae Carbapenem-Resistant (Sequence Type 258 [ST258] and ST11) and Hypervirulent (ST23, ST65, ST86, and ST375) Strains. J. Clin. Microbiol. 2018, 56, 731–749. [Google Scholar] [CrossRef]
- Gu, D.; Dong, N.; Zheng, Z.; Lin, D.; Huang, M.; Wang, L.; Chan, E.W.C.; Shu, L.; Yu, J.; Zhang, R.; et al. A Fatal Outbreak of ST11 Carbapenem-Resistant Hypervirulent Klebsiella pneumoniae in a Chinese Hospital: A Molecular Epidemiological Study. Lancet Infect. Dis. 2018, 18, 37–46. [Google Scholar] [CrossRef] [PubMed]
- Molton, J.S.; Chan, M.; Kalimuddin, S.; Oon, J.; Young, B.E.; Low, J.G.; Salada, B.M.A.; Lee, T.H.; Wijaya, L.; Fisher, D.A.; et al. Oral vs Intravenous Antibiotics for Patients with Klebsiella pneumoniae Liver Abscess: A Randomized, Controlled Noninferiority Study. Clin. Infect. Dis. 2020, 71, 952–959. [Google Scholar] [CrossRef] [PubMed]
- Jin, M.; Jia, T.; Liu, X.; Yang, M.; Zhang, N.; Chen, J.; Yang, X.; Qin, S.; Liu, F.; Tang, Y.; et al. Clinical and Genomic Analysis of Hypermucoviscous Klebsiella pneumoniae Isolates: Identification of New Hypermucoviscosity Associated Genes. Front. Cell Infect. Microbiol. 2023, 12, 1063406. [Google Scholar] [CrossRef] [PubMed]
- Wyres, K.L.; Wick, R.R.; Judd, L.M.; Froumine, R.; Tokolyi, A.; Gorrie, C.L.; Lam, M.M.C.; Duchêne, S.; Jenney, A.; Holt, K.E. Distinct Evolutionary Dynamics of Horizontal Gene Transfer in Drug Resistant and Virulent Clones of Klebsiella pneumoniae. PLoS Genet. 2019, 15, e1008114. [Google Scholar] [CrossRef] [PubMed]
- Cejas, D.; Canigia, L.F.; Cruz, G.R.; Elena, A.X.; Maldonado, I.; Gutkind, G.O.; Radice, M.A. First Isolate of KPC-2-Producing Klebsiella Pneumonaie Sequence Type 23 from the Americas. J. Clin. Microbiol. 2014, 52, 3483. [Google Scholar] [CrossRef] [PubMed]
- Saroj Khadka, A.; Ring, B.; Krzeminski, L.R.; Hathaway, M.; Walker, R.S.; Mobley, H.L.; Mike, L.A. Regulation of Klebsiella pneumoniae Mucoidy by the Bacterial Tyrosine Kinase Wzc. bioRxiv 2022. [Google Scholar] [CrossRef]
- Tanimoto, H.; Shigemura, K.; Osawa, K.; Kado, M.; Onishi, R.; Fang, S.B.; Sung, S.Y.; Miyara, T.; Fujisawa, M. Comparative Genetic Analysis of the Antimicrobial Susceptibilities and Virulence of Hypermucoviscous and Non-Hypermucoviscous ESBL-Producing Klebsiella pneumoniae in Japan. J. Microbiol. Immunol. Infect. 2023, 56, 93–103. [Google Scholar] [CrossRef] [PubMed]
- Shankar, C.; Nabarro, L.E.B.; Ragupathi, N.K.D.; Sethuvel, D.P.M.; Daniel, J.L.K.; Doss, C.G.P.; Veeraraghavan, B. Draft Genome Sequences of Three Hypervirulent Carbapenem-Resistant Klebsiella pneumoniae Isolates from Bacteremia. Genome Announc. 2016, 4, e01081-16. [Google Scholar] [CrossRef] [PubMed]
- Tang, M.; Kong, X.; Hao, J.; Liu, J. Epidemiological Characteristics and Formation Mechanisms of Multidrug-Resistant Hypervirulent Klebsiella pneumoniae. Front. Microbiol. 2020, 11, 581543. [Google Scholar] [CrossRef] [PubMed]
- Tian, D.; Liu, X.; Chen, W.; Zhou, Y.; Hu, D.; Wang, W.; Wu, J.; Mu, Q.; Jiang, X. Prevalence of Hypervirulent and Carbapenem-Resistant Klebsiella pneumoniae under Divergent Evolutionary Patterns. Emerg. Microbes Infect. 2022, 11, 1936–1949. [Google Scholar] [CrossRef] [PubMed]
- Gurieva, T.; Dautzenberg, M.J.D.; Gniadkowski, M.; Derde, L.P.G.; Bonten, M.J.M.; Bootsma, M.C.J. The Transmissibility of Antibiotic-Resistant Enterobacteriaceae in Intensive Care Units. Clin. Infect. Dis. 2018, 66, 489–493. [Google Scholar] [CrossRef]
- Wozniak, J.E.; Band, V.I.; Conley, A.B.; Rishishwar, L.; Burd, E.M.; Satola, S.W.; Hardy, D.J.; Tsay, R.; Farley, M.M.; Jacob, J.T.; et al. A Nationwide Screen of Carbapenem-Resistant Klebsiella pneumoniae Reveals an Isolate with Enhanced Virulence and Clinically Undetected Colistin Heteroresistance. Antimicrob. Agents Chemother. 2019, 63, e00107-19. [Google Scholar] [CrossRef] [PubMed]
- Harada, S.; Doia, Y. Hypervirulent Klebsiella pneumoniae: A Call for Consensus Definition and International Collaboration. J. Clin. Microbiol. 2018, 56, e00959-18. [Google Scholar] [CrossRef] [PubMed]
- Huynh, B.T.; Passet, V.; Rakotondrasoa, A.; Diallo, T.; Kerleguer, A.; Hennart, M.; De Lauzanne, A.; Herindrainy, P.; Seck, A.; Bercion, R.; et al. Klebsiella pneumoniae Carriage in Low-Income Countries: Antimicrobial Resistance, Genomic Diversity and Risk Factors. Gut Microbes 2020, 11, 1287–1299. [Google Scholar] [CrossRef] [PubMed]
- Gorrie, C.L.; Mirc Eta, M.; Wick, R.R.; Edwards, D.J.; Thomson, N.R.; Strugnell, R.A.; Pratt, N.F.; Garlick, J.S.; Watson, K.M.; Pilcher, D.V.; et al. Gastrointestinal Carriage Is a Major Reservoir of Klebsiella pneumoniae Infection in Intensive Care Patients. Clin. Infect. Dis. 2017, 65, 208–215. [Google Scholar] [CrossRef] [PubMed]
- Van Aartsen, J.J.; Moore, C.E.; Parry, C.M.; Turner, P.; Phot, N.; Mao, S.; Suy, K.; Davies, T.; Giess, A.; Sheppard, A.E.; et al. Epidemiology of Paediatric Gastrointestinal Colonisation by Extended Spectrum Cephalosporin-Resistant Escherichia Coli and Klebsiella pneumoniae Isolates in North-West Cambodia. BMC Microbiol. 2019, 19, 59. [Google Scholar] [CrossRef] [PubMed]
- Yam, E.L.Y.; Hsu, L.Y.; Yap, E.P.H.; Yeo, T.W.; Lee, V.; Schlundt, J.; Lwin, M.O.; Limmathurotsakul, D.; Jit, M.; Dedon, P.; et al. Antimicrobial Resistance in the Asia Pacific Region: A Meeting Report. Antimicrob. Resist. Infect. Control 2019, 8, 202. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.T.; Chen, T.L.; Siu, L.K.; Hsu, S.F.; Fung, C.P. Clinical and Microbiological Characteristics of Community-Acquired Thoracic Empyema or Complicated Parapneumonic Effusion Caused by Klebsiella pneumoniae in Taiwan. Eur. J. Clin. Microbiol. Infect. Dis. 2010, 29, 1003–1010. [Google Scholar] [CrossRef] [PubMed]
- Savelkoel, J.; Dance, D.A.B.; Currie, B.J.; Limmathurotsakul, D.; Wiersinga, W.J. A Call to Action: Time to Recognise Melioidosis as a Neglected Tropical Disease. Lancet Infect. Dis. 2022, 22, e176–e182. [Google Scholar] [CrossRef] [PubMed]
- Lam, M.M.C.; Wick, R.R.; Watts, S.C.; Cerdeira, L.T.; Wyres, K.L.; Holt, K.E. A Genomic Surveillance Framework and Genotyping Tool for Klebsiella pneumoniae and Its Related Species Complex. Nat. Commun. 2021, 12, 4188. [Google Scholar] [CrossRef] [PubMed]
- Pokharel, S.; Raut, S.; Adhikari, B. Tackling Antimicrobial Resistance in Low-Income and Middle-Income Countries. BMJ Glob. Health 2019, 4, e002104. [Google Scholar] [CrossRef] [PubMed]
- Savioli, L.; Daumerie, D. First WHO Report on Neglected Tropical Diseases: Working to Overcome the Global Impact of Neglected Tropical Diseases; WHO: Geneva, Switzerland, 2010. [Google Scholar]
- Raising Awareness of Melioidosis. Available online: https://www.melioidosis.info/infobox.aspx?pageID=101 (accessed on 22 January 2024).
- Kamau, E.; Ranson, E.L.; Tsan, A.T.; Bergmann-Leitner, E.S.; Garner, O.B.; Yang, S. Clinical and Genomic Characterization of Hypervirulent Klebsiella pneumoniae (HvKp) Infections via Passive Surveillance in Southern California, 2020–2022. Front Microbiol 2022, 13, 1001169. [Google Scholar] [CrossRef] [PubMed]
- Abani, O.; Abbas, A.; Abbas, F.; Abbas, M.; Abbasi, S.; Abbass, H.; Abbott, A.; Abdallah, N.; Abdelaziz, A.; Abdelfattah, M.; et al. Tocilizumab in Patients Admitted to Hospital with COVID-19 (RECOVERY): A Randomised, Controlled, Open-Label, Platform Trial. Lancet 2021, 397, 1637–1645. [Google Scholar] [CrossRef]
Phase | Antibiotic | Adult Dose | |
---|---|---|---|
Intensive | Meropenem | 1 g IV TDS (2 g TDS if neurological involvement) | |
Ceftazidime | 2 g IV QDS | ||
Eradication | Co-trimoxazole | 320 + 1600 mg PO BD (over 60 kg) | |
Amoxicillin-clavulanate | 20/mg/kg PO TDS | ||
Doxycycline | 100 mg PO BD |
Site of Infection | Minimum Intensive Phase Duration (Weeks) | Eradication Phase Duration (Months) |
---|---|---|
Cutaneous only | 2 | 3 |
Bacteraemia without focus | 2 | 3 |
Pneumonia without lymphadenopathy or ICU admission | 2 | 3 |
Pneumonia with lymphadenopathy or ICU admission | 4 | 3 |
Deep-seated collection | 4 (from the last drainage sample growing B. pseudomallei) | 3 |
Septic arthritis | 4 (from the last drainage sample growing B. pseudomallei) | 3 |
Osteomyelitis | 6 | 6 |
Central Nervous System infection | 8 | 6 |
Arterial infection or mycotic aneurysm | 8 | 6 |
A proxy for poverty and disadvantage; Affect populations with low visibility and little political voice; Do not travel widely; Cause stigma and discrimination, especially of girls and women; Have an important impact on morbidity and mortality; Are relatively neglected by research; Can be controlled, prevented, and possibly eliminated using effective and feasible solutions. |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kain, M.J.W.; Reece, N.L.; Parry, C.M.; Rajahram, G.S.; Paterson, D.L.; Woolley, S.D. The Rapid Emergence of Hypervirulent Klebsiella Species and Burkholderia pseudomallei as Major Health Threats in Southeast Asia: The Urgent Need for Recognition as Neglected Tropical Diseases. Trop. Med. Infect. Dis. 2024, 9, 80. https://doi.org/10.3390/tropicalmed9040080
Kain MJW, Reece NL, Parry CM, Rajahram GS, Paterson DL, Woolley SD. The Rapid Emergence of Hypervirulent Klebsiella Species and Burkholderia pseudomallei as Major Health Threats in Southeast Asia: The Urgent Need for Recognition as Neglected Tropical Diseases. Tropical Medicine and Infectious Disease. 2024; 9(4):80. https://doi.org/10.3390/tropicalmed9040080
Chicago/Turabian StyleKain, Matthew J. W., Nicola L. Reece, Christopher M. Parry, Giri Shan Rajahram, David L. Paterson, and Stephen D. Woolley. 2024. "The Rapid Emergence of Hypervirulent Klebsiella Species and Burkholderia pseudomallei as Major Health Threats in Southeast Asia: The Urgent Need for Recognition as Neglected Tropical Diseases" Tropical Medicine and Infectious Disease 9, no. 4: 80. https://doi.org/10.3390/tropicalmed9040080