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Article ; Online: High-depth sequencing characterization of viral dynamics across tissues in fatal COVID-19 reveals compartmentalized infection.

Normandin, Erica / Rudy, Melissa / Barkas, Nikolaos / Schaffner, Stephen F / Levine, Zoe / Padera, Robert F / Babadi, Mehrtash / Mukerji, Shibani S / Park, Daniel J / MacInnis, Bronwyn L / Siddle, Katherine J / Sabeti, Pardis C / Solomon, Isaac H

Nature communications

2023 Volume 14, Issue 1, Page(s) 574

Abstract: SARS-CoV-2 distribution and circulation dynamics are not well understood due to challenges in assessing genomic data from tissue samples. We develop experimental and computational workflows for high-depth viral sequencing and high-resolution genomic ... ...

Abstract	SARS-CoV-2 distribution and circulation dynamics are not well understood due to challenges in assessing genomic data from tissue samples. We develop experimental and computational workflows for high-depth viral sequencing and high-resolution genomic analyses from formalin-fixed, paraffin-embedded tissues and apply them to 120 specimens from six subjects with fatal COVID-19. To varying degrees, viral RNA is present in extrapulmonary tissues from all subjects. The majority of the 180 viral variants identified within subjects are unique to individual tissue samples. We find more high-frequency (>10%) minor variants in subjects with a longer disease course, with one subject harboring ten such variants, exclusively in extrapulmonary tissues. One tissue-specific high-frequency variant was a nonsynonymous mutation in the furin-cleavage site of the spike protein. Our findings suggest adaptation and/or compartmentalized infection, illuminating the basis of extrapulmonary COVID-19 symptoms and potential for viral reservoirs, and have broad utility for investigating human pathogens.
MeSH term(s)	Humans ; COVID-19 ; SARS-CoV-2/genetics ; SARS-CoV-2/metabolism ; Mutation ; Spike Glycoprotein, Coronavirus/genetics ; Spike Glycoprotein, Coronavirus/metabolism
Chemical Substances	Spike Glycoprotein, Coronavirus ; spike protein, SARS-CoV-2
Language	English
Publishing date	2023-02-02
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-022-34256-y
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Patient Acceptance of Routine Serial Postoperative Endoscopy Following Low Anterior Resection (LAR) and Its Ability to Detect Biomarkers in Anastomotic Lavage Fluid.

Guyton, Kristina / Belogortseva, Natalia / Levine, Zoe / Kaiser, Brooke Deatherage / Sangwan, Naseer / Hyman, Neil / Shogan, Benjamin D / Zaborina, Olga / Alverdy, John C

World journal of surgery

2021 Volume 45, Issue 7, Page(s) 2227–2234

Abstract: Background: Various reports have now established that postoperative endoscopy to examine and intervene in the process of anastomotic healing is both feasible and safe. Here we present our preliminary experience with serial postoperative endoscopy to ... ...

Abstract	Background: Various reports have now established that postoperative endoscopy to examine and intervene in the process of anastomotic healing is both feasible and safe. Here we present our preliminary experience with serial postoperative endoscopy to determine its feasibility, patient acceptance and the ability to obtain and the utility of perianastomotic material for molecular analysis. Methods: Patients undergoing LAR with ileostomy for rectal cancer were recruited for study to undergo routine serial endoscopic surveillance (SES) at three time points during the course of LAR: intraoperatively, before discharge (postoperative day 3-7) and at follow-up (postoperative day 10-28). At each endoscopy, images were captured, anastomotic tissues were lavaged and lavage fluid was retrieved. Fluid samples were analyzed using proteomics, zymography, ELISA and bacteria via 16S rRNA gene amplicon sequencing and culture of collagenolytic strains. Results: SES is feasible and acceptable to this limited set of patients following LAR. Biologic analysis of perianastomotic fluids was able to detect the presence of proteins, microbiota and inflammatory mediators previously identified at anastomotic sites in animals with pathologic healing. Conclusion: SES can be implemented in patients undergoing LAR with a high degree of patient compliance and capture of biologic information and imaging. Application of this approach has the potential to uncover, for the first time, the natural history of normal versus pathologic anastomotic healing in patients undergoing anastomotic surgery.
MeSH term(s)	Anastomosis, Surgical/adverse effects ; Anastomotic Leak/diagnosis ; Animals ; Biomarkers ; Endoscopy ; Humans ; RNA, Ribosomal, 16S ; Rectal Neoplasms/surgery ; Retrospective Studies ; Therapeutic Irrigation
Chemical Substances	Biomarkers ; RNA, Ribosomal, 16S
Language	English
Publishing date	2021-03-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	224043-9
ISSN	1432-2323 ; 0364-2313
ISSN (online)	1432-2323
ISSN	0364-2313
DOI	10.1007/s00268-021-06062-y
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Investigating the etiologies of non-malarial febrile illness in Senegal using metagenomic sequencing.

Nature communications

2024 Volume 15, Issue 1, Page(s) 747

Abstract: The worldwide decline in malaria incidence is revealing the extensive burden of non-malarial febrile illness (NMFI), which remains poorly understood and difficult to diagnose. To characterize NMFI in Senegal, we collected venous blood and clinical ... ...

Abstract	The worldwide decline in malaria incidence is revealing the extensive burden of non-malarial febrile illness (NMFI), which remains poorly understood and difficult to diagnose. To characterize NMFI in Senegal, we collected venous blood and clinical metadata in a cross-sectional study of febrile patients and healthy controls in a low malaria burden area. Using 16S and untargeted sequencing, we detected viral, bacterial, or eukaryotic pathogens in 23% (38/163) of NMFI cases. Bacteria were the most common, with relapsing fever Borrelia and spotted fever Rickettsia found in 15.5% and 3.8% of cases, respectively. Four viral pathogens were found in a total of 7 febrile cases (3.5%). Sequencing also detected undiagnosed Plasmodium, including one putative P. ovale infection. We developed a logistic regression model that can distinguish Borrelia from NMFIs with similar presentation based on symptoms and vital signs (F1 score: 0.823). These results highlight the challenge and importance of improved diagnostics, especially for Borrelia, to support diagnosis and surveillance.
MeSH term(s)	Humans ; Senegal/epidemiology ; Cross-Sectional Studies ; Malaria/diagnosis ; Malaria/epidemiology ; Plasmodium ; Fever/epidemiology ; Borrelia/genetics
Language	English
Publishing date	2024-01-25
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-024-44800-7
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Article ; Online: Comparative genetics of Enterococcus faecalis intestinal tissue isolates before and after surgery in a rat model of colon anastomosis.

Christley, Scott / Shogan, Benjamin / Levine, Zoe / Koo, Hyun / Guyton, Kristina / Owens, Sarah / Gilbert, Jack / Zaborina, Olga / Alverdy, John C

PloS one

2020 Volume 15, Issue 4, Page(s) e0232165

Abstract: We have recently demonstrated that collagenolytic Enterococcus faecalis plays a key and causative role in the pathogenesis of anastomotic leak, an uncommon but potentially lethal complication characterized by disruption of the intestinal wound following ... ...

Abstract	We have recently demonstrated that collagenolytic Enterococcus faecalis plays a key and causative role in the pathogenesis of anastomotic leak, an uncommon but potentially lethal complication characterized by disruption of the intestinal wound following segmental removal of the colon (resection) and its reconnection (anastomosis). Here we hypothesized that comparative genetic analysis of E. faecalis isolates present at the anastomotic wound site before and after surgery would shed insight into the mechanisms by which collagenolytic strains are selected for and predominate at sites of anastomotic disruption. Whole genome optical mapping of four pairs of isolates from rat colonic tissue obtained following surgical resection (herein named "pre-op" isolates) and then 6 days later from the anastomotic site (herein named "post-op" isolates) demonstrated that the isolates with higher collagenolytic activity formed a distinct cluster. In order to perform analysis at a deeper level, a single pair of E. faecalis isolates (16A pre-op and 16A post-op) was selected for whole genome sequencing and assembled using a hybrid assembly algorithm. Comparative genomics demonstrated absence of multiple gene clusters, notably a pathogenicity island in the post-op isolate. No differences were found in the fsr-gelE-sprE genes (EF1817-1822) responsible for regulation and production of collagenolytic activity. Analysis of unique genes among the 16A pre-op and post-op isolates revealed the predominance of transporter systems-related genes in the pre-op isolate and phage-related and hydrolytic enzyme-encoding genes in the post-op isolate. Despite genetic differences observed between pre-op and post-op isolates, the precise genetic determinants responsible for their differential expression of collagenolytic activity remains unknown.
MeSH term(s)	Anastomosis, Surgical/adverse effects ; Anastomotic Leak/etiology ; Anastomotic Leak/microbiology ; Animals ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Chromosome Mapping ; Collagenases/genetics ; Collagenases/metabolism ; Colon/surgery ; Enterococcus faecalis/enzymology ; Enterococcus faecalis/genetics ; Enterococcus faecalis/isolation & purification ; Gastrointestinal Microbiome/genetics ; Genome, Bacterial ; Intestines/microbiology ; Rats ; Virulence/genetics
Chemical Substances	Bacterial Proteins ; Collagenases (EC 3.4.24.-)
Language	English
Publishing date	2020-04-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0232165
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Article ; Online: Identification of Collagenolytic Bacteria in Human Samples: Screening Methods and Clinical Implications for Resolving and Preventing Anastomotic Leaks and Wound Complications.

Guyton, Kristina L / Levine, Zoe C / Lowry, Ann C / Lambert, Laura / Gribovskaja-Rupp, Irena / Hyman, Neil / Zaborina, Olga / Alverdy, John

Diseases of the colon and rectum

2019 Volume 62, Issue 8, Page(s) 972–979

Abstract: Background: Bacteria that produce collagen-digesting enzymes (collagenolytic bacteria) have been shown to play a critical and previously unappreciated role in anastomotic leak pathogenesis by breaking down host tissue extracellular matrix proteins. ... ...

Abstract	Background: Bacteria that produce collagen-digesting enzymes (collagenolytic bacteria) have been shown to play a critical and previously unappreciated role in anastomotic leak pathogenesis by breaking down host tissue extracellular matrix proteins. Detection of these bacteria is labor intensive, and no screening method currently exists. Objectives: We evaluated a rapid screening method developed to detect the presence of these collagenolytic bacteria in clinical samples, such as drain fluid, anastomotic tissue, or feces. Design: We compared a new method of detecting collagenolytic bacterial species with a previously used technique using samples from a murine experimental model and then demonstrated the utility of this screening method in samples from patients with anastomotic complications. Settings: All of the laboratory work and previous murine experiments were performed in Dr Alverdy's laboratory at the University of Chicago under institutional review board-approved protocols. Patients: Samples from patients with challenging wound complications were provided by participating clinicians with verbal patient consent. Given the small number of patients, this was determined to be institutional review board exempt. Main outcome measures: Whether this analysis can influence patient management and outcomes will require additional study. Results: This screening method detects numerous strains of bacteria with collagenolytic properties, including the collagenolytic species that have been implicated previously in anastomotic leak. Once collagenolytic strains are identified, they can be speciated and tested for antibiotic resistance using standard laboratory techniques. Limitations: This study is limited by the small number of patient samples tested. Conclusions: We demonstrated the potential applicability of this assay to evaluate rare and complex anastomotic complications that often require analysis beyond standard culture and sensitivity assays. Future applications of this method may allow the development of strategies to prevent anastomotic leak related to collagenolytic bacteria. See Video Abstract at http://links.lww.com/DCR/A962.
MeSH term(s)	Anastomotic Leak/microbiology ; Anastomotic Leak/prevention & control ; Antibiotic Prophylaxis/methods ; Bacteria/enzymology ; Bacteria/isolation & purification ; Colectomy/adverse effects ; Collagenases/analysis ; Colonic Diseases/surgery ; Female ; Humans ; Male ; Recurrence ; Retrospective Studies ; Surgical Wound Infection/microbiology ; Surgical Wound Infection/prevention & control
Chemical Substances	Collagenases (EC 3.4.24.-)
Language	English
Publishing date	2019-07-06
Publishing country	United States
Document type	Case Reports ; Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	212581-x
ISSN	1530-0358 ; 0012-3706
ISSN (online)	1530-0358
ISSN	0012-3706
DOI	10.1097/DCR.0000000000001417
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Article ; Online: Restructured Mitochondrial-Nuclear Interaction in Plasmodium falciparum Dormancy and Persister Survival after Artemisinin Exposure.

Connelly, Sean V / Manzella-Lapeira, Javier / Levine, Zoë C / Brzostowski, Joseph / Krymskaya, Ludmila / Rahman, Rifat S / Ellis, Angela C / Amin, Shuchi N / Sá, Juliana M / Wellems, Thomas E

mBio

2021 Volume 12, Issue 3, Page(s) e0075321

Abstract: Artemisinin and its semisynthetic derivatives (ART) are fast acting, potent antimalarials; however, their use in malaria treatment is frequently confounded by recrudescences from ... ...

Abstract	Artemisinin and its semisynthetic derivatives (ART) are fast acting, potent antimalarials; however, their use in malaria treatment is frequently confounded by recrudescences from bloodstream
MeSH term(s)	Antimalarials/pharmacology ; Artemisinins/pharmacology ; Cell Nucleus/metabolism ; Erythrocytes/drug effects ; Erythrocytes/parasitology ; Humans ; Malaria, Falciparum/parasitology ; Mitochondria/metabolism ; Plasmodium falciparum/drug effects ; Plasmodium falciparum/physiology
Chemical Substances	Antimalarials ; Artemisinins ; artenimol (6A9O50735X)
Language	English
Publishing date	2021-05-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mBio.00753-21
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Article: Improving diagnosis of non-malarial fevers in Senegal:

medRxiv : the preprint server for health sciences

2023

Abstract	The worldwide decline in malaria incidence is revealing the extensive burden of non-malarial febrile illness (NMFI), which remains poorly understood and difficult to diagnose. To characterize NMFI in Senegal, we collected venous blood and clinical metadata from febrile patients and healthy controls in a low malaria burden area. Using 16S and unbiased sequencing, we detected viral, bacterial, or eukaryotic pathogens in 29% of NMFI cases. Bacteria were the most common, with relapsing fever
Language	English
Publishing date	2023-08-25
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.08.24.23294564
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Article: The 2022 RSV surge was driven by multiple viral lineages.

medRxiv : the preprint server for health sciences

2023

Abstract: The US experienced an early and severe respiratory syncytial virus (RSV) surge in autumn 2022. Despite the pressure this has put on hospitals and care centers, the factors promoting the surge in cases are unknown. To investigate whether viral ... ...

Abstract	The US experienced an early and severe respiratory syncytial virus (RSV) surge in autumn 2022. Despite the pressure this has put on hospitals and care centers, the factors promoting the surge in cases are unknown. To investigate whether viral characteristics contributed to the extent or severity of the surge, we sequenced 105 RSV-positive specimens from symptomatic patients diagnosed with RSV who presented to the Massachusetts General Hospital (MGH) and its outpatient practices in the Greater Boston Area. Genomic analysis of the resulting 77 genomes (54 with >80% coverage, and 23 with >5% coverage) demonstrated that the surge was driven by multiple lineages of RSV-A (91%; 70/77) and RSV-B (9%; 7/77). Phylogenetic analysis of all US RSV-A revealed 12 clades, 4 of which contained Massachusetts and Washington genomes. These clades individually had times to most recent common ancestor (tMRCA) between 2014 and 2017, and together had a tMRCA of 2009, suggesting that they emerged well before the COVID-19 pandemic. Similarly, the RSV-B genomes had a tMRCA between 2016 and 2019. We found that the RSV-A and RSV-B genomes in our sample did not differ statistically from the estimated clock rate of the larger phylogenetic tree (10.6 and 12.4 substitutions per year, respectively). In summary, the polyphyletic nature of viral genomes sequenced in the US during the autumn 2022 surge is inconsistent with the emergence of a single, highly transmissible causal RSV lineage.
Language	English
Publishing date	2023-01-05
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.01.04.23284195
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Article ; Online: Viral Lineages in the 2022 RSV Surge in the United States.

The New England journal of medicine

2023 Volume 388, Issue 14, Page(s) 1335–1337

MeSH term(s)	Humans ; Infant ; Respiratory Syncytial Virus Infections/epidemiology ; Respiratory Syncytial Virus Infections/genetics ; Respiratory Syncytial Virus Infections/virology ; Seasons ; United States/epidemiology ; Disease Outbreaks ; Respiratory Syncytial Viruses/genetics
Language	English
Publishing date	2023-02-22
Publishing country	United States
Document type	Letter
ZDB-ID	207154-x
ISSN	1533-4406 ; 0028-4793
ISSN (online)	1533-4406
ISSN	0028-4793
DOI	10.1056/NEJMc2216153
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