<<

CONTENTS • SEPTEMBER 2020 • VOLUME 58, NO. 9

COVER IMAGE Cover photograph: See Photo Quiz at e00743-19. (Copyright © 2020 American Society for Microbiology. All Rights Reserved.)

PHOTO QUIZ Paul Bourbeau R Photo Quiz: A Farm Worker with Cavitary e00743-19 Photo Quiz Ashley M. Eckel, Lynda Bui, Ferric C. Fang Paul Bourbeau R Answer to Photo Quiz e00744-19 Photo Quiz Ashley M. Eckel, Lynda Bui, Ferric C. Fang

EDITORIAL Carey-Ann D. R Is This a Critical Result? A Micro-Comic Strip e01687-20 Burnham Editorial Alexander J. McAdam

THE BRIEF CASE Carey-Ann D. R The Brief Case: Secondary Measles and the Pitfalls of Diagnostic Testing e01938-19 Burnham Brief Case Marwan M. Azar, Joseph Canterino, Marie L. Landry Carey-Ann D. R Closing the Brief Case: Secondary Measles and the Pitfalls of Diagnostic Testing e01939-19 Burnham Brief Case Marwan M. Azar, Joseph Canterino, Marie L. Landry

BIOGRAPHICAL FEATURE Alexander J. R Biographical Feature: Robin Patel, M.D.(C.M.), D(ABMM), F(AAM), FIDSA, FACP e01259-20 McAdam Bio Feature Erik Munson

MINIREVIEWS Colleen Suzanne R Diagnostic Accuracy of Nucleic Acid Amplification-Based Assays for Clostridium e00363-20 Kraft Minireview perfringens-Associated Diseases: a Systematic Review and Meta-analysis Ke Chen, Sarfraz Ahmed, Yun-Juan Sheng, Changfeng Sun, Cun-Liang Deng, Suvash Chandra Ojha Bobbi S. Pritt R Role of Toxoplasma gondii IgG Avidity Testing in Discriminating between Acute e00505-20 Minireview and Chronic Toxoplasmosis in Pregnancy Aref Teimouri, Sina Mohtasebi, Elham Kazemirad, Hossein Keshavarz Colleen Suzanne R Fourth-Generation QuantiFERON-TB Gold Plus: What Is the Evidence? e01950-19 Kraft Minireview Arena Shafeque, Jacob Bigio, Catherine A. Hogan, Madhukar Pai, Niaz Banaei

BACTERIOLOGY John P. Dekker T Genomic Surveillance Enables Suitability Assessment of Salmonella Gene Targets e00038-20 Bacteriology Used for Culture-Independent Diagnostic Testing Rebecca J. Rockett, Alicia Arnott, Qinning Wang, Peter Howard, Vitali Sintchenko Erik Munson T A Population-Specific Optimized GeneXpert Pooling Algorithm for Chlamydia e00176-20 Bacteriology trachomatis and To Reduce Cost of Molecular Sexually Transmitted Infection Screening in Resource-Limited Settings Sarah Connolly, William Kilembe, Mubiana Inambao, Ana-Maria Visoiu, Tyronza Sharkey, Rachel Parker, Kristin M. Wall, Amanda Tichacek, Eric Hunter, Susan Allen

Instructions to Authors are available on the journal website. CONTENTS • SEPTEMBER 2020 • VOLUME 58, NO. 9

Brad Fenwick T Comparative Analysis of the Euroimmun CXCL13 Enzyme-Linked Immunosorbent e00207-20 Bacteriology Assay and the ReaScan Lateral Flow Immunoassay for Diagnosis of Lyme Neuroborreliosis Katharina Ziegler, Anca Rath, Christoph Schoerner, Renate Meyer, Thomas Bertsch, Frank Erbguth, Christian Bogdan, Jörg Steinmann, Jürgen Held Karen C. Carroll T Utilization, Yield, and Accuracy of the FilmArray Meningitis/Encephalitis Panel e00311-20 Bacteriology with Diagnostic Stewardship and Testing Algorithm M. Jana Broadhurst, Shefali Dujari, Indre Budvytiene, Benjamin A. Pinsky, Carl A. Gold, Niaz Banaei Karen C. Carroll T Impact of Rapid Antimicrobial Susceptibility Testing in Gram-Negative Rod e00360-20 Bacteriology Bacteremia: a Quasi-experimental Study Catherine Anne Hogan, Bertrand Ebunji, Nancy Watz, Kristopher Kapphahn, Joseph Rigdon, Emily Mui, Lina Meng, William Alegria, Marisa Holubar, Stanley Deresinski, Niaz Banaei Karen C. Carroll T Gold Standard Diagnostics Are Tarnished by Lytic Bacteriophage and e00412-20 Bacteriology E. J. Nelson, J. A. Grembi, D. L. Chao, J. R. Andrews, L. Alexandrova, P. H. Rodriguez, V. V. Ramachandran, M. A. Sayeed, J. F. Wamala, A. K. Debes, D. A. Sack, A. J. Hryckowian, F. Haque, S. Khatun, M. Rahman, A. Chien, A. M. Spormann, G. K. Schoolnik Nathan A. T Newly Named aerogenes (formerly Enterobacter aerogenes)Is e00582-20 Ledeboer Bacteriology Associated with Poor Clinical Outcomes Relative to Other Enterobacter Species in Patients with Bloodstream Infection Austin Wesevich, Granger Sutton, Felicia Ruffin, Lawrence P. Park, Derrick E. Fouts, Vance G. Fowler, Jr., Joshua T. Thaden Nathan A. T Multicenter Evaluation of the Xpert Carba-R Assay for Detection and e00644-20 Ledeboer Bacteriology Identification of Carbapenemase Genes in Sputum Specimens Zhen Cai, Jia Tao, Tianye Jia, Hongyu Fu, Xin Zhang, Mei Zhao, Hong Du, Hua Yu, Bin Shan, Bin Huang, Liang Chen, Yi-Wei Tang, Wei Jia, Fen Qu John P. Dekker T Comparative Genomics and Antimicrobial Resistance Profiling of Elizabethkingia e00730-20 Bacteriology Isolates Reveal Nosocomial Transmission and In Vitro Susceptibility to Fluoroquinolones, Tetracyclines, and Trimethoprim-Sulfamethoxazole Delaney Burnard, Letitia Gore, Andrew Henderson, Ama Ranasinghe, Haakon Bergh, Kyra Cottrell, Derek S. Sarovich, Erin P. Price, David L. Paterson, Patrick N. A. Harris Nathan A. T NitroSpeed-Carba NP Test for Rapid Detection and Differentiation between e00932-20 Ledeboer Bacteriology Different Classes of Carbapenemases in Patrice Nordmann, Mustafa Sadek, Anthony Demord, Laurent Poirel Nathan A. T A Selective Culture Medium for Screening Ceftazidime-Avibactam Resistance in e00965-20 Ledeboer Bacteriology Enterobacterales and Mustafa Sadek, Laurent Poirel, Camille Tinguely, Patrice Nordmann Brad Fenwick T Optimizing a Screening Protocol for Potential Extended-Spectrum ␤-Lactamase e01039-19 Bacteriology on MacConkey Agar for Use in a Global Surveillance Program Megan E. Jacob, Shivaramu Keelara, Awa Aidara-Kane, Jorge R. Matheu Alvarez, Paula J. Fedorka-Cray Erik Munson T Prevalence of Mycoplasma genitalium and Resistance-Associated Mutations in e01084-20 Bacteriology Patients at a Sexually Transmitted Infection Clinic in Iceland, and Comparison of the S-DiaMGTV and Aptima Mycoplasma genitalium Assays for Diagnosis Ingibjörg Hilmarsdóttir, Eva Mjöll Arnardóttir, Elísabet Reykdal Jóhannesdóttir, Freyja Valsdóttir, Daniel Golparian, Ronza Hadad, Hannes Bjarki Vigfússon, Magnus Unemo

September 2020 Volume 58 Issue 9 Journal of Clinical Microbiology jcm.asm.org iii CONTENTS • SEPTEMBER 2020 • VOLUME 58, NO. 9

Erik Munson T Changing from Clinician-Collected to Self-Collected Throat Swabs for Oropharyngeal e01215-20 Bacteriology and Chlamydia Screening among Men Who Have Sex with Men Eric P. F. Chow, Catriona S. Bradshaw, Deborah A. Williamson, Shauna Hall, Marcus Y. Chen, Tiffany R. Phillips, Ria Fortune, Kate Maddaford, Christopher K. Fairley Andrew B. T Mild or Malign: Clinical Characteristics and Outcomes of Clostridium difficile e01217-20 Onderdonk Bacteriology Infection in Thailand Korakrit Imwattana, Papanin Putsathit, Teera Leepattarakit, Pattarachai Kiratisin, Thomas V. Riley Karen C. Carroll T The Addition of Anaerobic Blood Cultures for Pediatric Patients with Concerns e01844-19 Bacteriology for Bloodstream Infections: Prevalence and Time to Positive Cultures Jennifer Dien Bard, Todd P. Chang, Rebecca Yee, Keya Manshadi, Nhan Lichtenfeld, Hee Jae Choi, Ara Festekjian Alexander J. T Performance of PCR/Electrospray Ionization-Mass Spectrometry on Whole e01860-19 McAdam Bacteriology Blood for Detection of Bloodstream Microorganisms in Patients with Suspected Kristoffer Strålin, Richard E. Rothman, Volkan Özenci, Kieron Barkataki, David Brealey, Neelam Dhiman, Lara Poling, Michael C. Kurz, Ajit P. Limaye, Frank LoVecchio, Kristin Lowery, Loren G. Miller, Gregory J. Moran, J. Scott Overcash, Amisha Parekh, W. Frank Peacock, Emanuel P. Rivers, Matthew Sims, Amy M. Stubbs, Martin Sundqvist, Måns Ullberg, Karen C. Carroll

CHLAMYDIOLOGY AND RICKETTSIOLOGY Daniel J. Diekema T Optimization and Evaluation of a Multiplex Quantitative PCR Assay for Detection e01802-19 Chlamyd Rickett of Nucleic Acids in Human Blood Samples from Patients with , Rickettsiosis, , Monocytic , and Granulocytic Megan E. Reller, J. Stephen Dumler

MYCOBACTERIOLOGY AND AEROBIC ACTINOMYCETES Melissa B. Miller T Accuracy of Xpert Ultra in Diagnosis of Pulmonary Tuberculosis among Children e00410-20 Mycobacteriology in Uganda: a Substudy from the SHINE Trial Willy Ssengooba, Jean de Dieu Iragena, Lydia Nakiyingi, Serestine Mujumbi, Eric Wobudeya, Robert Mboizi, David Boulware, David B. Meya, Louise Choo, Angela M. Crook, Kristen Lebeau, Moses Joloba, Anne-Marie Demers, Fiona V. Cresswell, Diana M. Gibb Melissa B. Miller T Evaluation of Xpert MTB/RIF Ultra Assay for Diagnosis of Childhood Tuberculosis: e00702-20 Mycobacteriology a Multicenter Accuracy Study Lin Sun, Yu Zhu, Min Fang, Yan Shi, Xiaoshan Peng, Qiong Liao, Xingyun Wang, Shuting Quan, Yacui Wang, Li Duan, Xiaomei Shi, Zhipeng Zhao, Lanqin Chen, Yongsheng Xu, Tongqiang Zhang, Xiaojian Cui, Chaomin Wan, Adong Shen

MYCOLOGY Kimberly E. HansonT Evaluation of a Novel Semiquantitative Cryptococcal Antigen Lateral Flow Assay e00441-20 Mycology in Patients with Advanced HIV Disease Joseph N. Jarvis, Mark W. Tenforde, Kwana Lechiile, Thandi Milton, Amber Boose, Tshepo B. Leeme, Leabaneng Tawe, Charles Muthoga, Ivy Rukasha, Fredah Mulenga, Ikanyeng Rulaganyang, Mooketsi Molefi, Síle F. Molloy, Julia Ngidi, Thomas S. Harrison, Nelesh P. Govender, Madisa Mine

iv jcm.asm.org Journal of Clinical Microbiology Volume 58 Issue 9 September 2020 CONTENTS • SEPTEMBER 2020 • VOLUME 58, NO. 9

VIROLOGY Yi-Wei Tang T Comparison of Serum Hepatitis B Virus RNA Levels and Quasispecies Evolution e00075-20 Virology Patterns between Entecavir and Pegylated-Interferon Mono-treatment in Chronic Hepatitis B Patients Xiao-qi Yu, Ming-jie Wang, De-min Yu, Pei-zhan Chen, Ming-yu Zhu, Wei Huang, Yue Han, Qi-ming Gong, Xin-xin Zhang Andrew B. T Evaluation of the FecalSwab for Stool Specimen Storage and Molecular Detection e00178-20 Onderdonk Virology of Enteropathogens on the BD Max System Melissa Richard-Greenblatt, Candy Rutherford, Kathy Luinstra, Ana María Cárdenas, Xiaoli Lilly Pang, Padman Jayaratne, Marek Smieja Yi-Wei Tang T Biennial Upsurge and Molecular Epidemiology of Enterovirus D68 Infection in e00284-20 Virology New York, USA, 2014 to 2018 Victoria L. Gilrane, Jian Zhuge, Weihua Huang, Sheila M. Nolan, Abhay Dhand, Changhong Yin, Christian Salib, Faariah Shakil, Helen Engel, John T. Fallon, Guiqing Wang Angela M. CaliendoT A Highly Prevalent Polymorphism in the Core Region Impairs Quantification of e00647-20 Virology Hepatitis B Virus (HBV) by the cobas TaqMan HBV Assay Laure Boizeau, Annabelle Servant-Delmas, Alexandra Ducancelle, Stéphane Chevaliez, Vincent Thibault, Syria Laperche, Pierre Cappy Yi-Wei Tang T Rapid and Sensitive Direct Detection and Identification of Poliovirus from Stool e00920-20 Virology and Environmental Surveillance Samples by Use of Nanopore Sequencing Alexander G. Shaw, Manasi Majumdar, Catherine Troman, Áine O’Toole, Blossom Benny, Dilip Abraham, Ira Praharaj, Gagandeep Kang, Salmaan Sharif, Muhammad Masroor Alam, Shahzad Shaukat, Mehar Angez, Adnan Khurshid, Nayab Mahmood, Yasir Arshad, Lubna Rehman, Ghulam Mujtaba, Ribqa Akthar, Muhammad Salman, Dimitra Klapsa, Yara Hajarha, Humayun Asghar, Ananda Bandyopadhyay, Andrew Rambaut, Javier Martin, Nicholas Grassly Angela M. CaliendoT Diagnostic Accuracy of Pan-Degenerate Amplification and Adaptation Assay e01045-20 Virology for HIV-1 Drug Resistance Mutation Analysis in Low- and Middle-Income Countries Vinie Kouamou, Justen Manasa, David Katzenstein, Alan M. McGregor, Chiratidzo E. Ndhlovu, Tariro Makadzange Alexander J. T Analytical and Clinical Comparison of Three Nucleic Acid Amplification Tests for e01134-20 McAdam Virology SARS-CoV-2 Detection Elizabeth Smith, Wei Zhen, Ryhana Manji, Deborah Schron, Scott Duong, Gregory J. Berry Angela M. CaliendoT Utility of Stool PCR for the Diagnosis of COVID-19: Comparison of Two e01369-20 Virology Commercial Platforms Wendy A. Szymczak, D. Yitzchak Goldstein, Erika P. Orner, Roger A. Fecher, Raquel T. Yokoda, Karin A. Skalina, Momka Narlieva, Inessa Gendlina, Amy S. Fox Melissa B. Miller T Clinical Evaluation of Self-Collected Saliva by Quantitative Reverse Transcription- e01438-20 Virology PCR (RT-qPCR), Direct RT-qPCR, Reverse Transcription–Loop-Mediated Isothermal Amplification, and a Rapid Antigen Test To Diagnose COVID-19 Mayu Nagura-Ikeda, Kazuo Imai, Sakiko Tabata, Kazuyasu Miyoshi, Nami Murahara, Tsukasa Mizuno, Midori Horiuchi, Kento Kato, Yoshitaka Imoto, Maki Iwata, Satoshi Mimura, Toshimitsu Ito, Kaku Tamura, Yasuyuki Kato

September 2020 Volume 58 Issue 9 Journal of Clinical Microbiology jcm.asm.org v CONTENTS • SEPTEMBER 2020 • VOLUME 58, NO. 9

Alexander J. T Direct Comparison of SARS-CoV-2 Analytical Limits of Detection across Seven e01535-20 McAdam Virology Molecular Assays Becky Fung, Allan Gopez, Venice Servellita, Shaun Arevalo, Coral Ho, Anne Deucher, Ed Thornborrow, Charles Chiu, Steve Miller

IMMUNOASSAYS Yi-Wei Tang T Development and Evaluation of a New Triplex Immunoassay That Detects Group e00300-20 Immunoassays A Streptococcus Antibodies for the Diagnosis of Rheumatic Fever Alana L. Whitcombe, Paulina Hanson-Manful, Susan Jack, Arlo Upton, Polly Atatoa Carr, Deborah A. Williamson, Michael G. Baker, Thomas Proft, Nicole J. Moreland Brad Fenwick T Evaluation of Serological Tests for Detection of Antibodies against Lumpy Skin e00348-20 Immunoassays Disease Virus Nina Krešic´, Ivana Šimic´, Tomislav Bedekovic´, Žaklin Acinger-Rogic´, Ivana Lojkic´ Yi-Wei Tang T Comparability of Titers of Antibodies against Seasonal Influenza Virus Strains as e00750-20 Immunoassays Determined by Hemagglutination Inhibition and Microneutralization Assays Marten Heeringa, Brett Leav, Igor Smolenov, Giuseppe Palladino, Leah Isakov, Vincent Matassa Melissa B. Miller T Clinical and Analytical Performance of an Automated Serological Test That e01224-20 Immunoassays Identifies S1/S2-Neutralizing IgG in COVID-19 Patients Semiquantitatively Fabrizio Bonelli, Antonella Sarasini, Claudia Zierold, Mariella Calleri, Alice Bonetti, Chiara Vismara, Frank A. Blocki, Luca Pallavicini, Alberto Chinali, Daniela Campisi, Elena Percivalle, Anna Pia DiNapoli, Carlo Federico Perno, Fausto Baldanti

EPIDEMIOLOGY John P. Dekker T Development and Application of a Core Genome Multilocus Sequence Typing e00214-20 Epidemiology Scheme for the Health Care-Associated Pathogen Pseudomonas aeruginosa Richard A. Stanton, Gillian McAllister, Jonathan B. Daniels, Erin Breaker, Nicholas Vlachos, Paige Gable, Heather Moulton-Meissner, Alison Laufer Halpin Daniel J. Diekema T Clinical and Genomic Epidemiology of Carbapenem-Nonsusceptible Citrobacter e00275-20 Epidemiology spp. at a Tertiary Health Care Center over 2 Decades Ahmed Babiker, Daniel R. Evans, Marissa P. Griffith, Christi L. McElheny, Mohamed Hassan, Lloyd G. Clarke, Roberta T. Mettus, Lee H. Harrison, Yohei Doi, Ryan K. Shields, Daria Van Tyne Alexander T Population Genomic Molecular Epidemiological Study of Macrolide-Resistant e00638-20 Mellmann Epidemiology Streptococcus pyogenes in Iceland, 1995 to 2016: Identification of a Large Clonal Population with a pbp2x Mutation Conferring Reduced In Vitro ␤-Lactam Susceptibility Sara B. Southon, Stephen B. Beres, Priyanka Kachroo, Matthew Ojeda Saavedra, Helga Erlendsdóttir, Gunnsteinn Haraldsson, Prasanti Yerramilli, Layne Pruitt, Luchang Zhu, James M. Musser, Karl G. Kristinsson

LETTERS TO THE EDITOR Yi-Wei Tang D Discriminative Potential of the Vitek MS In Vitro Diagnostic Device Regarding e00278-20 Letter influenzae and Haemophilus haemolyticus Sebastian Nürnberg, Heike Claus, Manuel Krone, Ulrich Vogel, Thiên-Trí Lâm Erik Munson D Genotyping of Mycoplasma genitalium Suggests De Novo Acquisition of e00641-20 Letter Antimicrobial Resistance in Queensland, Australia Emma L. Sweeney, Jacob Tickner, Cheryl Bletchly, Graeme R. Nimmo, David M. Whiley

vi jcm.asm.org Journal of Clinical Microbiology Volume 58 Issue 9 September 2020 CONTENTS • SEPTEMBER 2020 • VOLUME 58, NO. 9

Daniel J. Diekema D Performance Evaluation of Culture-Independent SYBR Green Candida auris e00690-20 Letter Quantitative PCR Diagnostics on Anterior Nares Surveillance Swabs Ourania Georgacopoulos, Natalie S. Nunnally, Ngoc Le, Colleen Lysen, Rory M. Welsh, Milena Kordalewska, David S. Perlin, Elizabeth L. Berkow, D. Joseph Sexton Daniel J. Diekema D Locus CauMT1 Provides a Higher-Resolution Alternative to Ribosomal Gene e01039-20 Letter Sequencing for Initial Candida auris Genotyping Santosh Katiyar, Tom Edlind Alexander J. D Under-allocation: Critical Supply Chain Hurdles Negatively Impact the Ability of e01160-20 McAdam Letter Community Hospitals To Perform Repeat SARS-CoV-2 Testing Susan M. Butler-Wu, Noah Wald-Dickler, Paul Holtom, Kenneth M. Zangwill, Tam T. Van Michael J. D When To Retest: an Examination of Repeat COVID-19 PCR Patterns in an e01179-20 Loeffelholz Letter Ambulatory Population Dina N. Greene, Jane A. Dickerson, Alexander L. Greninger, Robert L. Schmidt Nathan A. D Reporting Considerations for Cefepime-Susceptible and -Susceptible-Dose e01271-20 Ledeboer Letter Dependent Results for Carbapenemase-Producing Enterobacterales J. A. Fissel, M. L. Yarbrough, T. Tekle, C.-A. D. Burnham, P. J. Simner Melissa B. Miller D QuantiFERON-TB Gold Plus: High Qualitative and Quantitative Agreement e01436-20 Letter between Enzyme-Linked Immunosorbent Assay (ELISA) and Chemiluminescence Immunoassay (CLIA) Danilo Villalta, Paola Martelli, Anna Moratto, Elita Ligato, Roberto Giacomello, Sara El Idrissi El Hachimi

September 2020 Volume 58 Issue 9 Journal of Clinical Microbiology jcm.asm.org vii