Last data update: Apr 22, 2024. (Total: 46599 publications since 2009)
Records 1-30 (of 57 Records) |
Query Trace: Halpin AL [original query] |
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Differentiation of hypervirulent and classical Klebsiella pneumoniae with acquired drug resistance
Russo TA , Alvarado CL , Davies CJ , Drayer ZJ , Carlino-MacDonald U , Hutson A , Luo TL , Martin MJ , Corey BW , Moser KA , Rasheed JK , Halpin AL , McGann PT , Lebreton F . mBio 2024 e0286723 Hypervirulent Klebsiella pneumoniae (hvKp) is a concerning pathogen that can cause life-threatening infections in otherwise healthy individuals. Importantly, although strains of hvKp have been acquiring antimicrobial resistance, the effect on virulence is unclear. Therefore, it is of critical importance to determine whether a given antimicrobial resistant K. pneumoniae isolate is hypervirulent. This report determined which combination of genotypic and phenotypic markers could most accurately identify hvKp strains with acquired resistance. Both logistic regression and a machine-learning prediction model demonstrated that biomarker count alone was the strongest predictor. The presence of all five of the biomarkers iucA, iroB, peg-344, rmpA, and rmpA2 was most accurate (94%); the presence of ≥4 of these biomarkers was most sensitive (100%). Accurately identifying hvKp is vital for surveillance and research, and the availability of biomarker data could alert the clinician that hvKp is a consideration, which, in turn, would assist in optimizing patient care. |
Reply to Gonzales-Luna et al
Gargis AS , Karlsson M , Kamile Rasheed J , Kent AG , McKay SL , Paulick AL , Anderson KF , Adamczyk M , Campbell D , Korhonen LC , McAllister G , Vlachos N , Halpin AL , Lutgring JD , Guh AY , Clifford McDonald L , Elkins CA . Clin Infect Dis 2023 76 (11) 2039-2041 We thank Gonzales-Luna and colleagues [1] for their comments. We agree that laboratories must have access to accurate and standardized methods for antimicrobial susceptibility testing (AST) results to be clinically meaningful. The reference method for performing Clostridioides difficile AST is agar dilution according to Clinical and Laboratory Standards Institute (CLSI) guidelines [2]. The CLSI method for performing AST for anaerobic bacteria recommends that 5 μg/mL of hemin be incorporated into agar dilution plates and that the hemin stock solution should be protected from light and stored at 4°C–8°C for no longer than 1 month [2]. The susceptibility testing done by Gargis et al [3] was performed according to these guidelines, and the hemin stock solution was protected from light. | | Nevertheless, we read with interest the research in recent years [4–6] related to heme-dependent metronidazole resistance, including the reported association between isolates characterized as heme dependent and metronidazole resistant and the presence of a T to G mutation (PnimBG) in the −10 promoter region of the nitroimidazole reductase gene, nimB [5]. While Olaitan et al [5] found that not all heme-dependent metronidazole-resistant isolates contained the PnimBG mutation, Olaitan et al [5] indicate that most do; therefore, the presence of PnimBG may be predictive of resistance. We determined that the nimB mutation was present in 20% of our study isolates (116 of 593), of which 99% (115 of 116) belonged to RT027 (Table 1). The remaining isolate was RT014, the only RT014 isolate containing the PnimBG mutation among the 65 evaluated. |
Evidence review and recommendations for the implementation of genomics for antimicrobial resistance surveillance: reports from an international expert group
Baker KS , Jauneikaite E , Nunn JG , Midega JT , Atun R , Holt KE , Walia K , Howden BP , Tate H , Okeke IN , Carattoli A , Hsu LY , Hopkins KL , Muloi DM , Wheeler NE , Aanensen DM , Mason LCE , Rodgus J , Hendriksen RS , Essack SY , Egyir B , Halpin AL , MacCannell DR , Campos J , Srikantiah P , Feasey NA , Peacock SJ . Lancet Microbe 2023 4 (12) e1035-e1039 Nearly a century after the beginning of the antibiotic era, which has been associated with unparalleled improvements in human health and reductions in mortality associated with infection, the dwindling pipeline for new antibiotic classes coupled with the inevitable spread of antimicrobial resistance (AMR) poses a major global challenge. Historically, surveillance of bacteria with AMR typically relied on phenotypic analysis of isolates taken from infected individuals, which provides only a low-resolution view of the epidemiology behind an individual infection or wider outbreak. Recent years have seen increasing adoption of powerful new genomic technologies with the potential to revolutionise AMR surveillance by providing a high-resolution picture of the AMR profile of the bacteria causing infections and providing real-time actionable information for treating and preventing infection. However, many barriers remain to be overcome before genomic technologies can be adopted as a standard part of routine AMR surveillance around the world. Accordingly, the Surveillance and Epidemiology of Drug-resistant Infections Consortium convened an expert working group to assess the benefits and challenges of using genomics for AMR surveillance. In this Series, we detail these discussions and provide recommendations from the working group that can help to realise the massive potential benefits for genomics in surveillance of AMR. |
Genomics for antimicrobial resistance surveillance to support infection prevention and control in health-care facilities
Jauneikaite E , Baker KS , Nunn JG , Midega JT , Hsu LY , Singh SR , Halpin AL , Hopkins KL , Price JR , Srikantiah P , Egyir B , Okeke IN , Holt KE , Peacock SJ , Feasey NA . Lancet Microbe 2023 4 (12) e1040-e1046 Integration of genomic technologies into routine antimicrobial resistance (AMR) surveillance in health-care facilities has the potential to generate rapid, actionable information for patient management and inform infection prevention and control measures in near real time. However, substantial challenges limit the implementation of genomics for AMR surveillance in clinical settings. Through a workshop series and online consultation, international experts from across the AMR and pathogen genomics fields convened to review the evidence base underpinning the use of genomics for AMR surveillance in a range of settings. Here, we summarise the identified challenges and potential benefits of genomic AMR surveillance in health-care settings, and outline the recommendations of the working group to realise this potential. These recommendations include the definition of viable and cost-effective use cases for genomic AMR surveillance, strengthening training competencies (particularly in bioinformatics), and building capacity at local, national, and regional levels using hub and spoke models. |
Comparison of carbapenem-susceptible and carbapenem-resistant Enterobacterales at nine sites in the USA, 2013-2016: a resource for antimicrobial resistance investigators
Lutgring JD , Kent AG , Bowers JR , Jasso-Selles DE , Albrecht V , Stevens VA , Pfeiffer A , Barnes R , Engelthaler DM , Johnson JK , Gargis AS , Rasheed JK , Limbago BM , Elkins CA , Karlsson M , Halpin AL . Microb Genom 2023 9 (11) Carbapenem-resistant Enterobacterales (CRE) are an urgent public health threat. Genomic sequencing is an important tool for investigating CRE. Through the Division of Healthcare Quality Promotion Sentinel Surveillance system, we collected CRE and carbapenem-susceptible Enterobacterales (CSE) from nine clinical laboratories in the USA from 2013 to 2016 and analysed both phenotypic and genomic sequencing data for 680 isolates. We describe the molecular epidemiology and antimicrobial susceptibility testing (AST) data of this collection of isolates. We also performed a phenotype-genotype correlation for the carbapenems and evaluated the presence of virulence genes in Klebsiella pneumoniae complex isolates. These AST and genomic sequencing data can be used to compare and contrast CRE and CSE at these sites and serve as a resource for the antimicrobial resistance research community. |
Posttransfusion sepsis attributable to bacterial contamination in platelet collection set manufacturing facility, United States
Kracalik I , Kent AG , Villa CH , Gable P , Annambhotla P , McAllister G , Yokoe D , Langelier CR , Oakeson K , Noble-Wang J , Illoh O , Halpin AL , Eder AF , Basavaraju SV . Emerg Infect Dis 2023 29 (10) 1979-1989 During May 2018‒December 2022, we reviewed transfusion-transmitted sepsis cases in the United States attributable to polymicrobial contaminated apheresis platelet components, including Acinetobacter calcoaceticus‒baumannii complex or Staphylococcus saprophyticus isolated from patients and components. Transfused platelet components underwent bacterial risk control strategies (primary culture, pathogen reduction or primary culture, and secondary rapid test) before transfusion. Environmental samples were collected from a platelet collection set manufacturing facility. Seven sepsis cases from 6 platelet donations from 6 different donors were identified in patients from 6 states; 3 patients died. Cultures identified Acinetobacter calcoaceticus‒baumannii complex in 6 patients and 6 transfused platelets, S. saprophyticus in 4 patients and 4 transfused platelets. Whole-genome sequencing showed environmental isolates from the manufacturer were closely related genetically to patient and platelet isolates, indicating the manufacturer was the most probable source of recurrent polymicrobial contamination. Clinicians should maintain awareness of possible transfusion-transmitted sepsis even when using bacterial risk control strategies. |
Erratum: Vol. 71, No. 6.
Lambrou AS , Shirk P , Steele MK , Paul P , Paden CR , Cadwell B , Reese HE , Aoki Y , Hassell N , Caravas J , Kovacs NA , Gerhart JG , Ng HJ , Zheng XY , Beck A , Chau R , Cintron R , Cook PW , Gulvik CA , Howard D , Jang Y , Knipe K , Lacek KA , Moser KA , Paskey AC , Rambo-Martin BL , Nagilla RR , Rethchless AC , Schmerer MW , Seby S , Shephard SS , Stanton RA , Stark TJ , Uehara A , Unoarumhi Y , Bentz ML , Burhgin A , Burroughs M , Davis ML , Keller MW , Keong LM , Le SS , Lee JS , Madden Jr JC , Nobles S , Owouor DC , Padilla J , Sheth M , Wilson MM , Talarico S , Chen JC , Oberste MS , Batra D , McMullan LK , Halpin AL , Galloway SE , MacCannell DR , Kondor R , Barnes J , MacNeil A , Silk BJ , Dugan VG , Scobie HM , Wentworth DE . MMWR Morb Mortal Wkly Rep 2022 71 (14) 528 The report “Genomic Surveillance for SARS-CoV-2 Variants: Predominance of the Delta (B.1.617.2) and Omicron (B.1.1.529) Variants — United States, June 2021–January 2022” contained several errors. |
Dialysis Water Supply Faucet as Reservoir for Carbapenemase-Producing Pseudomonas aeruginosa
Prestel C , Moulton-Meissner H , Gable P , Stanton RA , Glowicz J , Franco L , McConnell M , Torres T , John D , Blackwell G , Yates R , Brown C , Reyes K , McAllister GA , Kunz J , Conners EE , Benedict KM , Kirby A , Mattioli M , Xu K , Gualandi N , Booth S , Novosad S , Arduino M , Halpin AL , Wells K , Walters MS . Emerg Infect Dis 2022 28 (10) 2069-2073 During June 2017-November 2019, a total 36 patients with carbapenem-resistant Pseudomonas aeruginosa harboring Verona-integron-encoded metallo-β-lactamase were identified in a city in western Texas, USA. A faucet contaminated with the organism, identified through environmental sampling, in a specialty care room was the likely source for infection in a subset of patients. |
Reference Susceptibility Testing and Genomic Surveillance of Clostridioides difficile, United States, 2012-17.
Gargis AS , Karlsson M , Paulick AL , Anderson KF , Adamczyk M , Vlachos N , Kent AG , McAllister GA , McKay SL , Halpin AL , Albrecht V , Campbell D , Korhonen L , Elkins CA , Rasheed JK , Guh AY , McDonald LC , Lutgring JD . Clin Infect Dis 2022 76 (5) 890-896 BACKGROUND: Antimicrobial susceptibility testing (AST) is not routinely performed for Clostridioides difficile and data evaluating minimum inhibitory concentrations (MICs) are limited. We performed AST and whole genome sequencing (WGS) for 593 C. difficile isolates collected between 2012-2017 through the Centers for Disease Control and Prevention's Emerging Infections Program. METHODS: MICs to six antimicrobial agents (ceftriaxone, clindamycin, meropenem, metronidazole, moxifloxacin, and vancomycin) were determined using the reference agar dilution method according to Clinical and Laboratory Standards Institute guidelines. WGS was performed on all isolates to detect the presence of genes or mutations previously associated with resistance. RESULTS: Among all isolates, 98.5% displayed a vancomycin MIC ≤ 2 μg/mL and 97.3% displayed a metronidazole MIC ≤ 2 μg/mL. Ribotype 027 (RT027) isolates displayed higher vancomycin MICs (MIC50: 2 μg/mL; MIC90: 2 μg/mL) than non-RT027 isolates (MIC50: 0.5 μg/mL; MIC90: 1 μg/mL) (P < 0.01). No vanA/B genes were detected. RT027 isolates also showed higher MICs to clindamycin and moxifloxacin and were more likely to harbor associated resistance genes or mutations. CONCLUSIONS: Elevated MICs to antibiotics used for treatment of C. difficile infection were rare and there was no increase in MICs over time. The lack of vanA/B genes or mutations consistently associated with elevated vancomycin MICs suggests there are multifactorial mechanisms of resistance. Ongoing surveillance of C. difficile using reference AST and WGS to monitor MIC trends and the presence of antibiotic resistance mechanisms is essential. |
Whole-Genome Sequencing Reveals Diversity of Carbapenem-Resistant Pseudomonas aeruginosa Collected through CDC's Emerging Infections Program, United States, 2016-2018.
Stanton RA , Campbell D , McAllister GA , Breaker E , Adamczyk M , Daniels JB , Lutgring JD , Karlsson M , Schutz K , Jacob JT , Wilson LE , Vaeth E , Li L , Lynfield R , Snippes Vagnone PM , Phipps EC , Hancock EB , Dumyati G , Tsay R , Cassidy PM , Mounsey J , Grass JE , Bulens SN , Walters MS , Halpin AL . Antimicrob Agents Chemother 2022 66 (9) e0049622 The CDC's Emerging Infections Program (EIP) conducted population- and laboratory-based surveillance of US carbapenem-resistant Pseudomonas aeruginosa (CRPA) from 2016 through 2018. To characterize the pathotype, 1,019 isolates collected through this project underwent antimicrobial susceptibility testing and whole-genome sequencing. Sequenced genomes were classified using the seven-gene multilocus sequence typing (MLST) scheme and a core genome (cg)MLST scheme was used to determine phylogeny. Both chromosomal and horizontally transmitted mechanisms of carbapenem resistance were assessed. There were 336 sequence types (STs) among the 1,019 sequenced genomes, and the genomes varied by an average of 84.7% of the cgMLST alleles used. Mutations associated with dysfunction of the porin OprD were found in 888 (87.1%) of the genomes and were correlated with carbapenem resistance, and a machine learning model incorporating hundreds of genetic variations among the chromosomal mechanisms of resistance was able to classify resistant genomes. While only 7 (0.1%) isolates harbored carbapenemase genes, 66 (6.5%) had acquired non-carbapenemase β-lactamase genes, and these were more likely to have OprD dysfunction and be resistant to all carbapenems tested. The genetic diversity demonstrates that the pathotype includes a variety of strains, and clones previously identified as high-risk make up only a minority of CRPA strains in the United States. The increased carbapenem resistance in isolates with acquired non-carbapenemase β-lactamase genes suggests that horizontally transmitted mechanisms aside from carbapenemases themselves may be important drivers of the spread of carbapenem resistance in P. aeruginosa. |
Differential neutralization and inhibition of SARS-CoV-2 variants by antibodies elicited by COVID-19 mRNA vaccines.
Wang L , Kainulainen MH , Jiang N , Di H , Bonenfant G , Mills L , Currier M , Shrivastava-Ranjan P , Calderon BM , Sheth M , Mann BR , Hossain J , Lin X , Lester S , Pusch EA , Jones J , Cui D , Chatterjee P , Jenks MH , Morantz EK , Larson GP , Hatta M , Harcourt JL , Tamin A , Li Y , Tao Y , Zhao K , Lacek K , Burroughs A , Wang W , Wilson M , Wong T , Park SH , Tong S , Barnes JR , Tenforde MW , Self WH , Shapiro NI , Exline MC , Files DC , Gibbs KW , Hager DN , Patel M , Halpin AL , McMullan LK , Lee JS , Xia H , Xie X , Shi PY , Davis CT , Spiropoulou CF , Thornburg NJ , Oberste MS , Dugan VG , Wentworth DE , Zhou B . Nat Commun 2022 13 (1) 4350 The evolution of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has resulted in the emergence of new variant lineages that have exacerbated the COVID-19 pandemic. Some of those variants were designated as variants of concern/interest (VOC/VOI) by national or international authorities based on many factors including their potential impact on vaccine-mediated protection from disease. To ascertain and rank the risk of VOCs and VOIs, we analyze the ability of 14 variants (614G, Alpha, Beta, Gamma, Delta, Epsilon, Zeta, Eta, Theta, Iota, Kappa, Lambda, Mu, and Omicron) to escape from mRNA vaccine-induced antibodies. The variants show differential reductions in neutralization and replication by post-vaccination sera. Although the Omicron variant (BA.1, BA.1.1, and BA.2) shows the most escape from neutralization, sera collected after a third dose of vaccine (booster sera) retain moderate neutralizing activity against that variant. Therefore, vaccination remains an effective strategy during the COVID-19 pandemic. |
Are vancomycin non-susceptible clostridioides difficile strains emerging
Lutgring JD , McKay SL , Gargis AS , Halpin AL , McDonald LC . Clin Infect Dis 2022 75 (9) 1677-1678 TO THE EDITORWe read with concern the report by Darkoh and colleagues describing vancomycin resistance in Clostridioides difficile isolates recovered from patients in Houston, Texas, and Nairobi, Kenya [1]. The authors suggested that vancomycin resistance, which they found to be common, may lead to therapeutic failure for patients infected with C. difficile and that routine antimicrobial susceptibility testing (AST) should be expanded. The authors report that 26% of C. difficile toxin gene-positive patients in Houston and 67% of sequential hospitalized patients in Nairobi with acute diarrhea had growth on primary screening media containing 4g/mL vancomycin. This alarmingly high proportion of a vancomycin resistant phenotype exceeds initial treatment failure rates reported in the literature [2], calling into question the reliability of these findings. |
Molecular Epidemiology of Carbapenem-Resistant Acinetobacter baumannii in the United States, 2013-2017.
McKay SL , Vlachos N , Daniels JB , Albrecht VS , Stevens VA , Rasheed JK , Johnson JK , Lutgring JD , Sjölund-Karlsson M , Halpin AL . Microb Drug Resist 2022 28 (6) 645-653 Healthcare-associated carbapenem-resistant Acinetobacter baumannii (CRAB) infections are a serious threat associated with global epidemic clones and a variety of carbapenemase gene classes. In this study, we describe the molecular epidemiology, including whole-genome sequencing analysis and antimicrobial susceptibility profiles of 92 selected, nonredundant CRAB collected through public health efforts in the United States from 2013 to 2017. Among the 92 isolates, the Oxford (OX) multilocus sequence typing scheme identified 30 sequence types (STs); the majority of isolates (n = 59, 64%) represented STs belonging to the international clonal complex 92 (CC92(OX)). Among these, ST208(OX) (n = 21) and ST281(OX) (n = 20) were the most common. All isolates carried an OXA-type carbapenemase gene, comprising 20 alleles. Ninety isolates (98%) encoded an intrinsic OXA-51-like enzyme; 67 (73%) harbored an additional acquired bla(OXA) gene, most commonly bla(OXA-23) (n = 45; 49%). Compared with isolates harboring only intrinsic oxacillinase genes, acquired bla(OXA) gene presence was associated with higher prevalence of resistance and a higher median minimum inhibitory concentration to the carbapenem imipenem (64 μg/mL vs. 8 μg/mL), and antibiotics from other drug classes, including penicillin, aminoglycosides, cephalosporins, and polymyxins. These data illustrate the wide distribution of CC92(OX) and high prevalence of acquired bla(OXA) carbapenemase genes among CRAB in the United States. |
Sentinel Surveillance Reveals Emerging Daptomycin-Resistant ST736 Enterococcus faecium and Multiple Mechanisms of Linezolid Resistance in Enterococci in the United States.
Gargis AS , Spicer LM , Kent AG , Zhu W , Campbell D , McAllister G , Ewing TO , Albrecht V , Stevens VA , Sheth M , Padilla J , Batra D , Johnson JK , Halpin AL , Rasheed JK , Elkins CA , Karlsson M , Lutgring JD . Front Microbiol 2021 12 807398 Enterococcus faecalis and faecium with resistance to daptomycin and/or linezolid are emerging globally. We present the genomic characterization of daptomycin- and linezolid-resistant E. faecalis and E. faecium surveillance isolates from the United States, 2013-2016. Daptomycin resistance was low among E. faecalis (2/364, 0.5%) and E. faecium (17/344, 5%). The majority (71%, 12/17) of daptomycin-resistant E. faecium isolates belonged to the emerging ST736 clone and contained mutations in liaFSR and cls previously associated with resistance. However, 1/2 E. faecalis and 3/17 E. faecium did not contain these mutations previously associated with daptomycin resistance. Linezolid resistance was rare among E. faecalis (1/364, 0.3%) and E. faecium (2/344, 0.6%). These two E. faecium isolates, one of which was also resistant to daptomycin and vancomycin, contained the 23S rRNA nucleotide mutation (G2576T) associated with linezolid resistance. Long-read sequencing revealed the linezolid-resistant E. faecalis isolate contained chromosomal- and plasmid-encoded copies of optrA. The chromosomal optrA was located on the recently described Tn6674 multiresistance transposon. The second copy of optrA was encoded on an ∼65 kb mosaic plasmid, with component regions sharing high sequence identity to optrA-encoding multiresistance plasmids of animal origin. The optrA-encoding plasmid contained open reading frames predicted to encode proteins associated with a pheromone-responsive plasmid transfer system, and filter mating experiments confirmed the plasmid was conjugative. Continued surveillance of enterococci is necessary to assess the prevalence and trends of daptomycin and linezolid resistance in the United States, characterize resistance mechanisms and how they transfer, and monitor for emerging sequence types associated with resistance. |
Genomic Surveillance for SARS-CoV-2 Variants: Predominance of the Delta (B.1.617.2) and Omicron (B.1.1.529) Variants - United States, June 2021-January 2022.
Lambrou AS , Shirk P , Steele MK , Paul P , Paden CR , Cadwell B , Reese HE , Aoki Y , Hassell N , Caravas J , Kovacs NA , Gerhart JG , Ng HJ , Zheng XY , Beck A , Chau R , Cintron R , Cook PW , Gulvik CA , Howard D , Jang Y , Knipe K , Lacek KA , Moser KA , Paskey AC , Rambo-Martin BL , Nagilla RR , Rethchless AC , Schmerer MW , Seby S , Shephard SS , Stanton RA , Stark TJ , Uehara A , Unoarumhi Y , Bentz ML , Burhgin A , Burroughs M , Davis ML , Keller MW , Keong LM , Le SS , Lee JS , Madden Jr JC , Nobles S , Owouor DC , Padilla J , Sheth M , Wilson MM , Talarico S , Chen JC , Oberste MS , Batra D , McMullan LK , Halpin AL , Galloway SE , MacCannell DR , Kondor R , Barnes J , MacNeil A , Silk BJ , Dugan VG , Scobie HM , Wentworth DE . MMWR Morb Mortal Wkly Rep 2022 71 (6) 206-211 Genomic surveillance is a critical tool for tracking emerging variants of SARS-CoV-2 (the virus that causes COVID-19), which can exhibit characteristics that potentially affect public health and clinical interventions, including increased transmissibility, illness severity, and capacity for immune escape. During June 2021-January 2022, CDC expanded genomic surveillance data sources to incorporate sequence data from public repositories to produce weighted estimates of variant proportions at the jurisdiction level and refined analytic methods to enhance the timeliness and accuracy of national and regional variant proportion estimates. These changes also allowed for more comprehensive variant proportion estimation at the jurisdictional level (i.e., U.S. state, district, territory, and freely associated state). The data in this report are a summary of findings of recent proportions of circulating variants that are updated weekly on CDC's COVID Data Tracker website to enable timely public health action.(†) The SARS-CoV-2 Delta (B.1.617.2 and AY sublineages) variant rose from 1% to >50% of viral lineages circulating nationally during 8 weeks, from May 1-June 26, 2021. Delta-associated infections remained predominant until being rapidly overtaken by infections associated with the Omicron (B.1.1.529 and BA sublineages) variant in December 2021, when Omicron increased from 1% to >50% of circulating viral lineages during a 2-week period. As of the week ending January 22, 2022, Omicron was estimated to account for 99.2% (95% CI = 99.0%-99.5%) of SARS-CoV-2 infections nationwide, and Delta for 0.7% (95% CI = 0.5%-1.0%). The dynamic landscape of SARS-CoV-2 variants in 2021, including Delta- and Omicron-driven resurgences of SARS-CoV-2 transmission across the United States, underscores the importance of robust genomic surveillance efforts to inform public health planning and practice. |
Extensively Drug-Resistant Carbapenemase-Producing Pseudomonas aeruginosa and Medical Tourism from the United States to Mexico, 2018-2019.
Kracalik I , Ham DC , McAllister G , Smith AR , Vowles M , Kauber K , Zambrano M , Rodriguez G , Garner K , Chorbi K , Cassidy PM , McBee S , Stoney RJ , Moser K , Villarino ME , Zazueta OE , Bhatnagar A , Sula E , Stanton RA , Brown AC , Halpin AL , Epstein L , Walters MS . Emerg Infect Dis 2022 28 (1) 51-61 Carbapenem-resistant Pseudomonas aeruginosa (CRPA) producing the Verona integron‒encoded metallo-β-lactamase (VIM) are highly antimicrobial drug-resistant pathogens that are uncommon in the United States. We investigated the source of VIM-CRPA among US medical tourists who underwent bariatric surgery in Tijuana, Mexico. Cases were defined as isolation of VIM-CRPA or CRPA from a patient who had an elective invasive medical procedure in Mexico during January 2018‒December 2019 and within 45 days before specimen collection. Whole-genome sequencing of isolates was performed. Thirty-eight case-patients were identified in 18 states; 31 were operated on by surgeon 1, most frequently at facility A (27/31 patients). Whole-genome sequencing identified isolates linked to surgeon 1 were closely related and distinct from isolates linked to other surgeons in Tijuana. Facility A closed in March 2019. US patients and providers should acknowledge the risk for colonization or infection after medical tourism with highly drug-resistant pathogens uncommon in the United States. |
Descriptive Evaluation of Antibody Responses to SARS-CoV-2 Infection in Plasma and Gingival Crevicular Fluid in a Nursing Home Cohort-Arkansas, June-August 2020.
Brown NE , Lyons AK , Schuh AJ , Stumpf MM , Harcourt JL , Tamin A , Rasheed MAU , Mills L , Lester SN , Thornburg NJ , Nguyen K , Costantini V , Vinjé J , Huang JY , Gilbert SE , Gable P , Bollinger S , Sabour S , Beshearse E , Surie D , Biedron C , Gregory CJ , Clemmons NS , Whitaker B , Coughlin MM , Seely KA , Garner K , Gulley T , Haney T , Kothari A , Patil N , Halpin AL , McDonald LC , Kutty PK , Brown AC . Infect Control Hosp Epidemiol 2021 43 (11) 1-24 OBJECTIVE: Characterize and compare SARS-CoV-2-specific immune responses in plasma and gingival crevicular fluid (GCF) from nursing home residents during and after natural infection. DESIGN: Prospective cohort. SETTING: Nursing home. PARTICIPANTS: SARS-CoV-2-infected nursing home residents. METHODS: A convenience sample of 14 SARS-CoV-2-infected nursing home residents, enrolled 4-13 days after real-time reverse transcription polymerase chain reaction diagnosis, were followed for 42 days. Post diagnosis, plasma SARS-CoV-2-specific pan-Immunoglobulin (Ig), IgG, IgA, IgM, and neutralizing antibodies were measured at 5 timepoints and GCF SARS-CoV-2-specific IgG and IgA were measured at 4 timepoints. RESULTS: All participants demonstrated immune responses to SARS-CoV-2 infection. Among 12 phlebotomized participants, plasma was positive for pan-Ig and IgG in all 12, neutralizing antibodies in 11, IgM in 10, and IgA in 9. Among 14 participants with GCF specimens, GCF was positive for IgG in 13 and IgA in 12. Immunoglobulin responses in plasma and GCF had similar kinetics; median times to peak antibody response was similar across specimen types (4 weeks for IgG; 3 weeks for IgA). Participants with pan-Ig, IgG, and IgA detected in plasma and GCF IgG remained positive through this evaluation's end 46-55 days post-diagnosis. All participants were viral culture negative by the first detection of antibodies. CONCLUSIONS: Nursing home residents had detectable SARS-CoV-2 antibodies in plasma and GCF after infection. Kinetics of antibodies detected in GCF mirrored those from plasma. Non-invasive GCF may be useful for detecting and monitoring immunologic responses in populations unable or unwilling to be phlebotomized. |
Investigation of Bacterial Infections Among Patients Treated With Umbilical Cord Blood-Derived Products Marketed as Stem Cell Therapies.
Hartnett KP , Powell KM , Rankin D , Gable P , Kim JJ , Spoto S , Breaker E , Hunter R , Dotson N , McAllister G , Stevens V , Halpin AL , Houston H , Epson E , Malarkey M , Mendoza M , McNeill L , Perkins KM . JAMA Netw Open 2021 4 (10) e2128615 IMPORTANCE: The number of clinics marketing stem cell products for joint diseases, chronic pain, and most recently, COVID-19, has increased despite warnings from the US Food and Drug Administration that stem cell products for these and other indications have not been proven safe or effective. OBJECTIVE: To examine bacterial infections in 20 patients who received umbilical cord blood-derived products marketed as stem cell treatment. DESIGN, SETTING, AND PARTICIPANTS: This case series is a national public health investigation including case-finding, medical record review and abstraction, and laboratory investigation, including sterility testing of products and whole-genome sequencing of patient and product isolates. Participants included patients who developed bacterial infections following administration of umbilical cord blood-derived products marketed as stem cell treatment during August 2017 to September 2018. Data analysis was performed from March 2019 to September 2021. EXPOSURES: Umbilical cord blood-derived products marketed as stem cell treatment. MAIN OUTCOMES AND MEASURES: Data were collected on patient infections and exposures. The Centers for Disease Control and Prevention performed sterility testing on undistributed and distributed vials of product marketed as stem cell treatment and performed whole-genome sequencing to compare patient and product bacterial isolates. RESULTS: Culture-confirmed bacterial infections were identified in 20 patients (median [range] age, 63 [2-89] years; 13 male patients [65%]) from 8 US states who sought stem cell treatment for conditions including pain, osteoarthritis, rheumatoid arthritis, and injury; all but 1 required hospitalization. The most frequently isolated bacteria from patients with infections were common enteric species, including Escherichia coli (14 patients) and Enterobacter cloacae (7 patients). Of unopened, undistributed products sampled for testing, 65% (22 of 34 vials) were contaminated with at least 1 of 16 bacterial species, mostly enteric. A patient isolate from Arizona matched isolates obtained from products administered to patients in Florida, and patient isolates from Texas matched undistributed product sent from the company in California. CONCLUSIONS AND RELEVANCE: Unapproved stem cell products can expose patients to serious risks without proven benefit. Sequencing results suggest a common source of extensive contamination, likely occurring during the processing of cord blood into product. Patients and health care practitioners who are considering the use of unapproved products marketed as stem cell treatment should be aware of their unproven benefits and potential risks, including serious infections. |
Detection and Characterization of Targeted Carbapenem-Resistant Healthcare-Associated Threats: Findings from The Antibiotic Resistance Laboratory Network, 2017-2019.
Sabour S , Huang JY , Bhatnagar A , Gilbert SE , Karlsson M , Lonsway D , Lutgring JD , Rasheed JK , Halpin AL , Stanton RA , Gumbis S , Elkins CA , Brown AC . Antimicrob Agents Chemother 2021 65 (12) Aac0110521 Carbapenemase gene-positive (CP) Gram-negative bacilli are of significant clinical and public health concern. Their rapid detection and containment are critical to preventing their spread and additional infections they can cause. To this end, CDC developed the Antibiotic Resistance Laboratory Network (AR Lab Network), in which public health laboratories across all 50 states, several cities, and Puerto Rico characterize clinical isolates of carbapenem-resistant Enterobacterales (CRE), Pseudomonas aeruginosa (CRPA), and Acinetobacter baumannii (CRAB), and conduct colonization screens to detect the presence of mobile carbapenemase genes. In its first three years, the AR Lab Network tested 76,887 isolates and 31,001 rectal swab colonization screens. Targeted carbapenemase genes (bla(KPC), bla(NDM), bla(OXA-48-like), bla(VIM), or bla(IMP)) were detected by PCR in 35% of CRE, 2% of CRPA, <1% of CRAB, and 8% of colonization screens tested, respectively. bla(KPC) and bla(VIM) were the most common CP-CRE and CP-CRPA, respectively, but regional differences in the frequency of carbapenemase genes detected were apparent. In CRE and CRPA isolates tested for carbapenemase production and the presence of the targeted genes, 97% had concordant results; 3% of CRE and 2% of CRPA were carbapenemase production-positive but PCR-negative for those genes. Isolates harboring bla(NDM) showed the highest frequency of resistance across the carbapenems tested and those harboring bla(IMP) and bla(OXA-48-like) genes showed the lowest frequency of carbapenem resistance. The AR Lab Network provides a national snapshot of rare and emerging carbapenemase genes, delivering data to inform public health actions to limit the spread of these antibiotic resistance threats. |
The Effect of Disinfectants on the Microbial Community on Environmental Healthcare Surfaces using Next Generation Sequencing.
Perry-Dow KA , de Man T , Halpin AL , Shams AM , Rose LJ , Noble-Wang JA . Am J Infect Control 2021 50 (1) 54-60 BACKGROUND: Healthcare-associated infections (HAIs) are a significant economic burden and cause of avoidable morbidity and mortality within healthcare systems. The contribution of environmental contamination to HAI transmission has been recognized, but the mechanisms by which transmission occurs are still being investigated. The objective of this study was to characterize the microbial communities of disinfected, non-critical healthcare surfaces using next generation sequencing technology. METHODS: Composite environmental surface samples were from high-touch surfaces in rooms of patients isolated for infections with multidrug-resistant organisms during their hospitalization. Information on the disinfectant product used and cleaning type (routine or terminal) was collected. 16S rRNA gene amplicon sequencing and analysis were performed. Community analysis was conducted to determine the bacterial composition and compare the detection of target pathogens by culture from 94 Contact Precaution rooms. RESULTS: Overall percent agreement between culture and sequence methods ranged from 52% to 88%. A significant difference was observed in bacterial composition between rooms cleaned with bleach and those cleaned with a quaternary ammonium compound (QAC) for composite 2 (overbed table, intravenous pole, and inner room door handle) (ANOSIM R2 = 0.66, p = 0.005) but not composite 1 (bed rails, television remote control unit, call buttons, and telephone). CONCLUSIONS: Surfaces in bleach-cleaned rooms contained a higher proportion of gram-positive microbiota, whereas rooms cleaned with QAC contained a higher proportion of gram-negative microbiota, suggesting disinfectant products may impact the healthcare environment microbiome. |
GAMMA: a tool for the rapid identification, classification, and annotation of translated gene matches from sequencing data.
Stanton RA , Vlachos N , Halpin AL . Bioinformatics 2021 38 (2) 546-548 MOTIVATION: Tools used to identify genes in microbial sequences using a reference database generally report matches as a percent identity, which can be difficult to interpret in cases with <100%sequence identity, as changes to specific amino acids can have dramatic effects on protein function, such as when they occur in substrate binding regions or enzyme active sites, which in turn can have dramatic effects on phenotypes like antimicrobial resistance or virulence. RESULTS: Here we present GAMMA, an open-source tool for Gene Allele Mutation Microbial Assessment, which uses protein coding-level identity to make gene calls from any gene database and generates a classification (e.g., mutant, truncation) and translated annotation (e.g., Y190S mutation, truncation at residue 110) for these calls. GAMMA accurately called antimicrobial resistance genes from a large set of genomes faster than three other tools. It can also be used with any gene database, as we demonstrated by identifying virulence genes in the same genome set. Because of its speed and flexibility, GAMMA can be used to rapidly find and annotate any gene matches of interest in microbial sequencing data. AVAILABILITY: GAMMA is freely available as a Bioconda package (https://bioconda.github.io/recipes/gamma/README.html) and as a command line script (https://github.com/rastanton/GAMMA). SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online. |
Genomic Surveillance for SARS-CoV-2 Variants Circulating in the United States, December 2020-May 2021.
Paul P , France AM , Aoki Y , Batra D , Biggerstaff M , Dugan V , Galloway S , Hall AJ , Johansson MA , Kondor RJ , Halpin AL , Lee B , Lee JS , Limbago B , MacNeil A , MacCannell D , Paden CR , Queen K , Reese HE , Retchless AC , Slayton RB , Steele M , Tong S , Walters MS , Wentworth DE , Silk BJ . MMWR Morb Mortal Wkly Rep 2021 70 (23) 846-850 SARS-CoV-2, the virus that causes COVID-19, is constantly mutating, leading to new variants (1). Variants have the potential to affect transmission, disease severity, diagnostics, therapeutics, and natural and vaccine-induced immunity. In November 2020, CDC established national surveillance for SARS-CoV-2 variants using genomic sequencing. As of May 6, 2021, sequences from 177,044 SARS-CoV-2-positive specimens collected during December 20, 2020-May 6, 2021, from 55 U.S. jurisdictions had been generated by or reported to CDC. These included 3,275 sequences for the 2-week period ending January 2, 2021, compared with 25,000 sequences for the 2-week period ending April 24, 2021 (0.1% and 3.1% of reported positive SARS-CoV-2 tests, respectively). Because sequences might be generated by multiple laboratories and sequence availability varies both geographically and over time, CDC developed statistical weighting and variance estimation methods to generate population-based estimates of the proportions of identified variants among SARS-CoV-2 infections circulating nationwide and in each of the 10 U.S. Department of Health and Human Services (HHS) geographic regions.* During the 2-week period ending April 24, 2021, the B.1.1.7 and P.1 variants represented an estimated 66.0% and 5.0% of U.S. SARS-CoV-2 infections, respectively, demonstrating the rise to predominance of the B.1.1.7 variant of concern(†) (VOC) and emergence of the P.1 VOC in the United States. Using SARS-CoV-2 genomic surveillance methods to analyze surveillance data produces timely population-based estimates of the proportions of variants circulating nationally and regionally. Surveillance findings demonstrate the potential for new variants to emerge and become predominant, and the importance of robust genomic surveillance. Along with efforts to characterize the clinical and public health impact of SARS-CoV-2 variants, surveillance can help guide interventions to control the COVID-19 pandemic in the United States. |
Framing Bacterial Genomics for Public Health(care).
Halpin AL , McDonald LC , Elkins CA . J Clin Microbiol 2021 59 (12) Jcm0013521 Advancements in comparative genomics have generated significant interest in defining applications for healthcare-associated pathogens. Clinical microbiology, however, relies on increasingly automated platforms to quickly identify pathogens, resistance mechanisms, and therapy options within CLIA- and FDA-approved frameworks. Additionally, and most notably, healthcare-associated pathogens, especially those that are resistant to antibiotics, represent a diverse spectrum of genera harboring complex genetic targets including antibiotic, biocide, and virulence determinants that can be highly transmissible and, at least for antibiotic resistance, serve as potential targets for containment efforts. U.S. public health investments have focused on rapidly detecting outbreaks and emerging resistance in healthcare-associated pathogens using reference, culture-based, and molecular methods that are distributed, for example, across national laboratory network infrastructures. Herein we describe the public health applications of genomic science that are built from the top-down for broad surveillance, as well as the bottom-up, starting with identification of infections and infectious clusters. For healthcare-associated, including antimicrobial-resistant, pathogens, we propose a combination of top-down and bottom-up genomic approaches leveraged across the public health spectrum, from local infection control, to regional and national containment efforts, to national surveillance for understanding emerging strain ecology and fitness of healthcare pathogens. |
A Comparison of Less Invasive SARS-CoV-2 Diagnostic Specimens in Nursing Home Residents - Arkansas, June-August 2020.
Gable P , Huang JY , Gilbert SE , Bollinger S , Lyons AK , Sabour S , Surie D , Biedron C , Haney T , Beshearse E , Gregory CJ , Seely KA , Clemmons NS , Patil N , Kothari A , Gulley T , Garner K , Anderson K , Thornburg NJ , Halpin AL , McDonald LC , Kutty PK , Brown AC . Clin Infect Dis 2021 73 S58-S64 BACKGROUND: SARS-CoV-2 testing remains essential for early identification and clinical management of cases. We compared the diagnostic performance of three specimen types for characterizing SARS-CoV-2 in infected nursing home residents. METHODS: A convenience sample of 17 residents were enrolled within 15 days of first positive SARS-CoV-2 result by real-time reverse transcription polymerase chain reaction (RT-PCR) and prospectively followed for 42 days. Anterior nasal swabs (AN), oropharyngeal swabs (OP), and saliva specimens (SA) were collected on the day of enrollment, every 3 days for the first 21 days, then weekly for 21 days. Specimens were tested for presence of SARS-CoV-2 RNA using RT-PCR and replication-competent virus by viral culture. RESULTS: Comparing the three specimen types collected from each participant at each time point, the concordance of paired RT-PCR results ranged from 80-88%. After the first positive result, SA and OP were RT-PCR-positive for ≤48 days; AN were RT-PCR-positive for ≤33 days. AN had the highest percentage of RT-PCR-positive results (81%; 21/26) when collected ≤10 days of participants' first positive result. Eleven specimens were positive by viral culture: nine AN collected ≤19 days following first positive result and two OP collected ≤5 days following first positive result. CONCLUSIONS: AN, OP, and SA were effective methods for repeated testing in this population. More AN than OP were positive by viral culture. SA and OP remained RT-PCR-positive longer than AN, which could lead to unnecessary interventions if RT-PCR detection occurred after viral shedding has likely ceased. |
A Comprehensive Approach to Ending an Outbreak of Rare bla OXA-72 gene-positive Carbapenem-resistant Acinetobacter baumannii at a Community Hospital, Kansas City, MO, 2018
McKinsey DS , Gasser C , McKinsey JP , Ditto G , Agard A , Zellmer B , Poteete C , Vagnone PS , Dale JL , Bos J , Hahn R , Turabelidze G , Poiry M , Franklin P , Vlachos N , McAllister GA , Halpin AL , Glowicz J , Ham DC , Epstein L . Am J Infect Control 2021 49 (9) 1183-1185 We identified a cluster of extensively drug-resistant, carbapenemase gene-positive, carbapenem-resistant Acinetobacter baumannii (CP-CRAB) at a teaching hospital in Kansas City. Extensively drug-resistant CRAB was identified from eight patients and 3% of environmental cultures. We used patient cohorting and targeted environmental disinfection to stop transmission. After implementation of these measures, no additional cases were identified. |
Infectious Period of Severe Acute Respiratory Syndrome Coronavirus 2 in 17 Nursing Home Residents-Arkansas, June-August 2020.
Surie D , Huang JY , Brown AC , Gable P , Biedron C , Gilbert SE , Garner K , Bollinger S , Gulley T , Haney T , Lyons AK , Beshearse E , Gregory CJ , Sabour S , Clemmons NS , James AE , Tamin A , Reese N , Perry-Dow KA , Brown R , Harcourt JL , Campbell D , Houston H , Chakravorty R , Paulick A , Whitaker B , Murdoch J , Spicer L , Stumpf MM , Mills L , Coughlin MM , Higdem P , Rasheed MAU , Lonsway D , Bhatnagar A , Kothari A , Anderson K , Thornburg NJ , Breaker E , Adamczyk M , McAllister GA , Halpin AL , Seely KA , Patil N , McDonald LC , Kutty PK . Open Forum Infect Dis 2021 8 (3) ofab048 BACKGROUND: To estimate the infectious period of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in older adults with underlying conditions, we assessed duration of coronavirus disease 2019 (COVID-19) symptoms, reverse-transcription polymerase chain reaction (RT-PCR) positivity, and culture positivity among nursing home residents. METHODS: We enrolled residents within 15 days of their first positive SARS-CoV-2 test (diagnosis) at an Arkansas facility from July 7 to 15, 2020 and instead them for 42 days. Every 3 days for 21 days and then weekly, we assessed COVID-19 symptoms, collected specimens (oropharyngeal, anterior nares, and saliva), and reviewed medical charts. Blood for serology was collected on days 0, 6, 12, 21, and 42. Infectivity was defined by positive culture. Duration of culture positivity was compared with duration of COVID-19 symptoms and RT-PCR positivity. Data were summarized using measures of central tendency, frequencies, and proportions. RESULTS: We enrolled 17 of 39 (44%) eligible residents. Median participant age was 82 years (range, 58-97 years). All had ≥3 underlying conditions. Median duration of RT-PCR positivity was 22 days (interquartile range [IQR], 8-31 days) from diagnosis; median duration of symptoms was 42 days (IQR, 28-49 days). Of 9 (53%) participants with any culture-positive specimens, 1 (11%) severely immunocompromised participant remained culture-positive 19 days from diagnosis; 8 of 9 (89%) were culture-positive ≤8 days from diagnosis. Seroconversion occurred in 12 of 12 (100%) surviving participants with ≥1 blood specimen; all participants were culture-negative before seroconversion. CONCLUSIONS: Duration of infectivity was considerably shorter than duration of symptoms and RT-PCR positivity. Severe immunocompromise may prolong SARS-CoV-2 infectivity. Seroconversion indicated noninfectivity in this cohort. |
The State of Microbiome Science at the Intersection of Infectious Diseases and Antimicrobial Resistance.
Ranallo RT , McDonald LC , Halpin AL , Hiltke T , Young VB . J Infect Dis 2021 223 S187-S193 Along with the rise in modern chronic diseases, ranging from diabetes to asthma, lay the challenges posed by increasing antibiotic resistance resulting in difficult to treat infections, as well as sepsis. An emerging and unifying theme in the pathogenesis of these diverse public health threats is changes in the microbial communities that inhabit multiple body sites. Although there is great promise in exploring the role of these microbial communities in chronic disease pathogenesis, the shorter timeframe of most infectious disease pathogenesis may allow early translation of our basic scientific understanding of microbial ecology and host-microbiota-pathogen interactions. Likely translation avenues include development of preventive strategies, diagnostics, and therapeutics. For example, as basic research related to microbial pathogenesis continues to progress, Clostridioides difficile infection (CDI) is already being addressed clinically through at least two of these three avenues: targeted antibiotic stewardship and treatment of recurrent disease through fecal microbiota transplantation (FMT). |
Characterization of Clostridioides difficile Isolates Available through the CDC & FDA Antibiotic Resistance Isolate Bank.
Paulick A , Adamczyk M , Anderson K , Vlachos N , Machado MJ , McAllister G , Korhonen L , Guh AY , Halpin AL , Rasheed JK , Karlsson M , Lutgring JD , Gargis AS . Microbiol Resour Announc 2021 10 (1) Thirty Clostridioides difficile isolates collected in 2016 through the Centers for Disease Control and Prevention Emerging Infections Program were selected for reference antimicrobial susceptibility testing and whole-genome sequencing. Here, we present the genetic characteristics of these isolates and announce their availability in the CDC & FDA Antibiotic Resistance Isolate Bank. |
Transmission of novel Klebsiella pneumoniae carbapenemase-producing Escherichia coli sequence type 1193 among residents and caregivers in a community-based, residential care setting - Nevada, 2018
Gomes DJ , Bardossy AC , Chen L , Forero A , Gorzalski A , Holmstadt H , Causey K , Njoku C , Stone ND , Ogundimu A , Moulton-Meissner H , McAllister G , Halpin AL , Gable P , Vlachos N , Larson S , Walters MS , Epstein L . Infect Control Hosp Epidemiol 2020 41 (11) 1-3 We describe transmission of Klebsiella pneumoniae carbapenemase-producing Escherichia coli sequence type (ST) 1193 in a group home. E. coli ST1193 is an emerging multidrug-resistant clone not previously shown to carry carbapenemases in the United States. Our investigation illustrates the potential of residential group homes to amplify rare combinations of pathogens and resistance mechanisms. |
Development and application of a core genome multilocus sequence typing scheme for the healthcare-associated pathogen Pseudomonas aeruginosa .
Stanton RA , McAllister G , Daniels JB , Breaker E , Vlachos N , Gable P , Moulton-Meissner H , Halpin AL . J Clin Microbiol 2020 58 (9) Pseudomonas aeruginosa is an opportunistic human pathogen that frequently causes healthcare-associated infections (HAIs). Due to its metabolic diversity and ability to form biofilms, this gram negative, non-fermenter can persist in the healthcare environment, which can lead to prolonged HAI outbreaks. We describe the creation of a core genome MLST (cgMLST) scheme to provide a stable platform for the rapid comparison of P. aeruginosa isolates using whole genome sequencing (WGS) data. We used a diverse set of 58 complete P. aeruginosa genomes to curate a set of 4400 core genes found in each isolate, representing approximately 65% of the average genome size. We then expanded the alleles for each gene using 1991 contig-level genome sequences. The scheme was used to analyze genomes from four historical HAI outbreaks to compare the phylogenies generated using cgMLST to those of other means (traditional MLST, PFGE, and SNV analysis). The cgMLST scheme provides sufficient resolution for analyzing individual outbreaks, as well as the stability for comparisons across a variety of isolates encountered in surveillance studies, making it a valuable tool for the rapid analysis of P. aeruginosa genomes. |
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