Pharyngeal microbial signatures are predictive of the risk of fungal pneumonia in hematologic patients

Claudio Costantini; Emilia Nunzi; Angelica Spolzino; Melissa Palmieri; Giorgia Renga; Teresa Zelante; Lukas Englmaier; Katerina Coufalikova; Zdenek Spácil; Monica Borghi; Marina M. Bellet; Enzo Acerbi; Matteo Puccetti; Stefano Giovagnoli; Roberta Spaccapelo; Vincenzo N. Talesa; Giuseppe Lomurno; Francesco Merli; Luca Facchini; Antonio Spadea; Lorella Melillo; Katia Codeluppi; Francesco Marchesi; Gessica Marchesini; Daniela Valente; Giulia Dragonetti; Gianpaolo Nadali; Livio Pagano; Franco Aversa; Luigina Romani

doi:10.1128/IAI.00105-21

Pharyngeal microbial signatures are predictive of the risk of fungal pneumonia in hematologic patients

Claudio Costantini, Emilia Nunzi, Angelica Spolzino, Melissa Palmieri, Giorgia Renga, Teresa Zelante, Lukas Englmaier, Katerina Coufalikova, Zdenek Spácil, Monica Borghi, Marina M. Bellet, Enzo Acerbi, Matteo Puccetti, Stefano Giovagnoli, Roberta Spaccapelo, Vincenzo N. Talesa, Giuseppe Lomurno, Francesco Merli, Luca Facchini, Antonio SpadeaLorella Melillo, Katia Codeluppi, Francesco Marchesi, Gessica Marchesini, Daniela Valente, Giulia Dragonetti, Gianpaolo Nadali, Livio Pagano, Franco Aversa, Luigina Romani

Risultato della ricerca: Contributo in rivista › Articolo in rivista

Abstract

The ability to predict invasive fungal infections (IFI) in patients with hematological malignancies is fundamental for successful therapy. Although gut dysbiosis is known to occur in hematological patients, whether airway dysbiosis also contributes to the risk of IFI has not been investigated. Nasal and oropharyngeal swabs were collected for functional microbiota characterization in 173 patients with hematological malignancies recruited in a multicenter, prospective, observational study and stratified according to the risk of developing IFI. A lower microbial richness and evenness were found in the pharyngeal microbiota of high-risk patients that were associated with a distinct taxonomic and metabolic profile. A murine model of IFI provided biologic plausibility for the finding that loss of protective anaerobes, such as Clostridiales and Bacteroidetes, along with an apparent restricted availability of tryptophan, is causally linked to the risk of IFI in hematologic patients and indicates avenues for antimicrobial stewardship and metabolic reequilibrium in IFI.

Lingua originale	English
pagine (da-a)	e0010521-e0010538
Numero di pagine	17
Rivista	Infection and Immunity
Volume	89
DOI	https://doi.org/10.1128/IAI.00105-21
Stato di pubblicazione	Pubblicato - 2021

Keywords

Airway microbiome
Animals
Antibiotics
Antifungal Agents
Disease Models, Animal
Hematologic Diseases
Hematologic Neoplasms
Hematological malignancies
Humans
Indole-3aldehyde
Invasive fungal infection
Metabolomics
Metagenome
Metagenomics
Mice
Microbiota
Mycoses
Pharynx
Pneumonia
Risk Assessment
Risk Factors
Tryptophan

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10.1128/IAI.00105-21

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Costantini, C., Nunzi, E., Spolzino, A., Palmieri, M., Renga, G., Zelante, T., Englmaier, L., Coufalikova, K., Spácil, Z., Borghi, M., Bellet, M. M., Acerbi, E., Puccetti, M., Giovagnoli, S., Spaccapelo, R., Talesa, V. N., Lomurno, G., Merli, F., Facchini, L., ... Romani, L. (2021). Pharyngeal microbial signatures are predictive of the risk of fungal pneumonia in hematologic patients. Infection and Immunity, 89, e0010521-e0010538. https://doi.org/10.1128/IAI.00105-21

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title = "Pharyngeal microbial signatures are predictive of the risk of fungal pneumonia in hematologic patients",

abstract = "The ability to predict invasive fungal infections (IFI) in patients with hematological malignancies is fundamental for successful therapy. Although gut dysbiosis is known to occur in hematological patients, whether airway dysbiosis also contributes to the risk of IFI has not been investigated. Nasal and oropharyngeal swabs were collected for functional microbiota characterization in 173 patients with hematological malignancies recruited in a multicenter, prospective, observational study and stratified according to the risk of developing IFI. A lower microbial richness and evenness were found in the pharyngeal microbiota of high-risk patients that were associated with a distinct taxonomic and metabolic profile. A murine model of IFI provided biologic plausibility for the finding that loss of protective anaerobes, such as Clostridiales and Bacteroidetes, along with an apparent restricted availability of tryptophan, is causally linked to the risk of IFI in hematologic patients and indicates avenues for antimicrobial stewardship and metabolic reequilibrium in IFI.",

keywords = "Airway microbiome, Animals, Antibiotics, Antifungal Agents, Disease Models, Animal, Hematologic Diseases, Hematologic Neoplasms, Hematological malignancies, Humans, Indole-3aldehyde, Invasive fungal infection, Metabolomics, Metagenome, Metagenomics, Mice, Microbiota, Mycoses, Pharynx, Pneumonia, Risk Assessment, Risk Factors, Tryptophan, Airway microbiome, Animals, Antibiotics, Antifungal Agents, Disease Models, Animal, Hematologic Diseases, Hematologic Neoplasms, Hematological malignancies, Humans, Indole-3aldehyde, Invasive fungal infection, Metabolomics, Metagenome, Metagenomics, Mice, Microbiota, Mycoses, Pharynx, Pneumonia, Risk Assessment, Risk Factors, Tryptophan",

author = "Claudio Costantini and Emilia Nunzi and Angelica Spolzino and Melissa Palmieri and Giorgia Renga and Teresa Zelante and Lukas Englmaier and Katerina Coufalikova and Zdenek Sp{\'a}cil and Monica Borghi and Bellet, {Marina M.} and Enzo Acerbi and Matteo Puccetti and Stefano Giovagnoli and Roberta Spaccapelo and Talesa, {Vincenzo N.} and Giuseppe Lomurno and Francesco Merli and Luca Facchini and Antonio Spadea and Lorella Melillo and Katia Codeluppi and Francesco Marchesi and Gessica Marchesini and Daniela Valente and Giulia Dragonetti and Gianpaolo Nadali and Livio Pagano and Franco Aversa and Luigina Romani",

year = "2021",

doi = "10.1128/IAI.00105-21",

language = "English",

volume = "89",

pages = "e0010521--e0010538",

journal = "Infection and Immunity",

issn = "0019-9567",

publisher = "American Society for Microbiology",

}

Costantini, C, Nunzi, E, Spolzino, A, Palmieri, M, Renga, G, Zelante, T, Englmaier, L, Coufalikova, K, Spácil, Z, Borghi, M, Bellet, MM, Acerbi, E, Puccetti, M, Giovagnoli, S, Spaccapelo, R, Talesa, VN, Lomurno, G, Merli, F, Facchini, L, Spadea, A, Melillo, L, Codeluppi, K, Marchesi, F, Marchesini, G, Valente, D, Dragonetti, G, Nadali, G, Pagano, L, Aversa, F & Romani, L 2021, 'Pharyngeal microbial signatures are predictive of the risk of fungal pneumonia in hematologic patients', Infection and Immunity, vol. 89, pagg. e0010521-e0010538. https://doi.org/10.1128/IAI.00105-21

TY - JOUR

T1 - Pharyngeal microbial signatures are predictive of the risk of fungal pneumonia in hematologic patients

AU - Costantini, Claudio

AU - Nunzi, Emilia

AU - Spolzino, Angelica

AU - Palmieri, Melissa

AU - Renga, Giorgia

AU - Zelante, Teresa

AU - Englmaier, Lukas

AU - Coufalikova, Katerina

AU - Spácil, Zdenek

AU - Borghi, Monica

AU - Bellet, Marina M.

AU - Acerbi, Enzo

AU - Puccetti, Matteo

AU - Giovagnoli, Stefano

AU - Spaccapelo, Roberta

AU - Talesa, Vincenzo N.

AU - Lomurno, Giuseppe

AU - Merli, Francesco

AU - Facchini, Luca

AU - Spadea, Antonio

AU - Melillo, Lorella

AU - Codeluppi, Katia

AU - Marchesi, Francesco

AU - Marchesini, Gessica

AU - Valente, Daniela

AU - Dragonetti, Giulia

AU - Nadali, Gianpaolo

AU - Pagano, Livio

AU - Aversa, Franco

AU - Romani, Luigina

PY - 2021

Y1 - 2021

N2 - The ability to predict invasive fungal infections (IFI) in patients with hematological malignancies is fundamental for successful therapy. Although gut dysbiosis is known to occur in hematological patients, whether airway dysbiosis also contributes to the risk of IFI has not been investigated. Nasal and oropharyngeal swabs were collected for functional microbiota characterization in 173 patients with hematological malignancies recruited in a multicenter, prospective, observational study and stratified according to the risk of developing IFI. A lower microbial richness and evenness were found in the pharyngeal microbiota of high-risk patients that were associated with a distinct taxonomic and metabolic profile. A murine model of IFI provided biologic plausibility for the finding that loss of protective anaerobes, such as Clostridiales and Bacteroidetes, along with an apparent restricted availability of tryptophan, is causally linked to the risk of IFI in hematologic patients and indicates avenues for antimicrobial stewardship and metabolic reequilibrium in IFI.

AB - The ability to predict invasive fungal infections (IFI) in patients with hematological malignancies is fundamental for successful therapy. Although gut dysbiosis is known to occur in hematological patients, whether airway dysbiosis also contributes to the risk of IFI has not been investigated. Nasal and oropharyngeal swabs were collected for functional microbiota characterization in 173 patients with hematological malignancies recruited in a multicenter, prospective, observational study and stratified according to the risk of developing IFI. A lower microbial richness and evenness were found in the pharyngeal microbiota of high-risk patients that were associated with a distinct taxonomic and metabolic profile. A murine model of IFI provided biologic plausibility for the finding that loss of protective anaerobes, such as Clostridiales and Bacteroidetes, along with an apparent restricted availability of tryptophan, is causally linked to the risk of IFI in hematologic patients and indicates avenues for antimicrobial stewardship and metabolic reequilibrium in IFI.

KW - Airway microbiome

KW - Animals

KW - Antibiotics

KW - Antifungal Agents

KW - Disease Models, Animal

KW - Hematologic Diseases

KW - Hematologic Neoplasms

KW - Hematological malignancies

KW - Humans

KW - Indole-3aldehyde

KW - Invasive fungal infection

KW - Metabolomics

KW - Metagenome

KW - Metagenomics

KW - Mice

KW - Microbiota

KW - Mycoses

KW - Pharynx

KW - Pneumonia

KW - Risk Assessment

KW - Risk Factors

KW - Tryptophan

KW - Airway microbiome

KW - Animals

KW - Antibiotics

KW - Antifungal Agents

KW - Disease Models, Animal

KW - Hematologic Diseases

KW - Hematologic Neoplasms

KW - Hematological malignancies

KW - Humans

KW - Indole-3aldehyde

KW - Invasive fungal infection

KW - Metabolomics

KW - Metagenome

KW - Metagenomics

KW - Mice

KW - Microbiota

KW - Mycoses

KW - Pharynx

KW - Pneumonia

KW - Risk Assessment

KW - Risk Factors

KW - Tryptophan

UR - http://hdl.handle.net/10807/196881

U2 - 10.1128/IAI.00105-21

DO - 10.1128/IAI.00105-21

M3 - Article

SN - 0019-9567

VL - 89

SP - e0010521-e0010538

JO - Infection and Immunity

JF - Infection and Immunity

ER -

Pharyngeal microbial signatures are predictive of the risk of fungal pneumonia in hematologic patients

Abstract

Keywords

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