Postoperative Staphylococcus aureus Infections in Patients With and Without Preoperative Colonization

ASPIRE-SSI Study Team; Darren P R Troeman; Derek Hazard; Leen Timbermont; Surbhi Malhotra-Kumar; Cornelis H van Werkhoven; Martin Wolkewitz; Alexey Ruzin; Herman Goossens; Marc J M Bonten; Stephan Harbarth; Frangiscos Sifakis; Jan A J W Kluytmans

doi:10.1001/jamanetworkopen.2023.39793

Postoperative Staphylococcus aureus Infections in Patients With and Without Preoperative Colonization

ASPIRE-SSI Study Team, Darren P R Troeman^*, Derek Hazard, Leen Timbermont, Surbhi Malhotra-Kumar, Cornelis H van Werkhoven, Martin Wolkewitz, Alexey Ruzin, Herman Goossens, Marc J M Bonten, Stephan Harbarth, Frangiscos Sifakis, Jan A J W Kluytmans

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

IMPORTANCE: Staphylococcus aureus surgical site infections (SSIs) and bloodstream infections (BSIs) are important complications of surgical procedures for which prevention remains suboptimal. Contemporary data on the incidence of and etiologic factors for these infections are needed to support the development of improved preventive strategies.

OBJECTIVES: To assess the occurrence of postoperative S aureus SSIs and BSIs and quantify its association with patient-related and contextual factors.

DESIGN, SETTING, AND PARTICIPANTS: This multicenter cohort study assessed surgical patients at 33 hospitals in 10 European countries who were recruited between December 16, 2016, and September 30, 2019 (follow-up through December 30, 2019). Enrolled patients were actively followed up for up to 90 days after surgery to assess the occurrence of S aureus SSIs and BSIs. Data analysis was performed between November 20, 2020, and April 21, 2022. All patients were 18 years or older and had undergone 11 different types of surgical procedures. They were screened for S aureus colonization in the nose, throat, and perineum within 30 days before surgery (source population). Both S aureus carriers and noncarriers were subsequently enrolled in a 2:1 ratio.

EXPOSURE: Preoperative S aureus colonization.

MAIN OUTCOMES AND MEASURES: The main outcome was cumulative incidence of S aureus SSIs and BSIs estimated for the source population, using weighted incidence calculation. The independent association of candidate variables was estimated using multivariable Cox proportional hazards regression models.

RESULTS: In total, 5004 patients (median [IQR] age, 66 [56-72] years; 2510 [50.2%] female) were enrolled in the study cohort; 3369 (67.3%) were S aureus carriers. One hundred patients developed S aureus SSIs or BSIs within 90 days after surgery. The weighted cumulative incidence of S aureus SSIs or BSIs was 2.55% (95% CI, 2.05%-3.12%) for carriers and 0.52% (95% CI, 0.22%-0.91%) for noncarriers. Preoperative S aureus colonization (adjusted hazard ratio [AHR], 4.38; 95% CI, 2.19-8.76), having nonremovable implants (AHR, 2.00; 95% CI, 1.15-3.49), undergoing mastectomy (AHR, 5.13; 95% CI, 1.87-14.08) or neurosurgery (AHR, 2.47; 95% CI, 1.09-5.61) (compared with orthopedic surgery), and body mass index (AHR, 1.05; 95% CI, 1.01-1.08 per unit increase) were independently associated with S aureus SSIs and BSIs.

CONCLUSIONS AND RELEVANCE: In this cohort study of surgical patients, S aureus carriage was associated with an increased risk of developing S aureus SSIs and BSIs. Both modifiable and nonmodifiable etiologic factors were associated with this risk and should be addressed in those at increased S aureus SSI and BSI risk.

Original language	English
Pages (from-to)	e2339793
Journal	Jama network open
Volume	6
Issue number	10
DOIs	https://doi.org/10.1001/jamanetworkopen.2023.39793
Publication status	Published - 2-Oct-2023
Externally published	Yes

Keywords

Aged
Female
Humans
Male
Breast Neoplasms/complications
Cohort Studies
Mastectomy
Staphylococcal Infections/prevention & control
Staphylococcus aureus
Surgical Wound Infection/prevention & control
Middle Aged

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ASPIRE-SSI Study Team, Troeman, D. P. R., Hazard, D., Timbermont, L., Malhotra-Kumar, S., van Werkhoven, C. H., Wolkewitz, M., Ruzin, A., Goossens, H., Bonten, M. J. M., Harbarth, S., Sifakis, F., & Kluytmans, J. A. J. W. (2023). Postoperative Staphylococcus aureus Infections in Patients With and Without Preoperative Colonization. Jama network open, 6(10), e2339793. https://doi.org/10.1001/jamanetworkopen.2023.39793

@article{12ef5bb159d44d74b39f662057fd4d37,

title = "Postoperative Staphylococcus aureus Infections in Patients With and Without Preoperative Colonization",

abstract = "IMPORTANCE: Staphylococcus aureus surgical site infections (SSIs) and bloodstream infections (BSIs) are important complications of surgical procedures for which prevention remains suboptimal. Contemporary data on the incidence of and etiologic factors for these infections are needed to support the development of improved preventive strategies.OBJECTIVES: To assess the occurrence of postoperative S aureus SSIs and BSIs and quantify its association with patient-related and contextual factors.DESIGN, SETTING, AND PARTICIPANTS: This multicenter cohort study assessed surgical patients at 33 hospitals in 10 European countries who were recruited between December 16, 2016, and September 30, 2019 (follow-up through December 30, 2019). Enrolled patients were actively followed up for up to 90 days after surgery to assess the occurrence of S aureus SSIs and BSIs. Data analysis was performed between November 20, 2020, and April 21, 2022. All patients were 18 years or older and had undergone 11 different types of surgical procedures. They were screened for S aureus colonization in the nose, throat, and perineum within 30 days before surgery (source population). Both S aureus carriers and noncarriers were subsequently enrolled in a 2:1 ratio.EXPOSURE: Preoperative S aureus colonization.MAIN OUTCOMES AND MEASURES: The main outcome was cumulative incidence of S aureus SSIs and BSIs estimated for the source population, using weighted incidence calculation. The independent association of candidate variables was estimated using multivariable Cox proportional hazards regression models.RESULTS: In total, 5004 patients (median [IQR] age, 66 [56-72] years; 2510 [50.2%] female) were enrolled in the study cohort; 3369 (67.3%) were S aureus carriers. One hundred patients developed S aureus SSIs or BSIs within 90 days after surgery. The weighted cumulative incidence of S aureus SSIs or BSIs was 2.55% (95% CI, 2.05%-3.12%) for carriers and 0.52% (95% CI, 0.22%-0.91%) for noncarriers. Preoperative S aureus colonization (adjusted hazard ratio [AHR], 4.38; 95% CI, 2.19-8.76), having nonremovable implants (AHR, 2.00; 95% CI, 1.15-3.49), undergoing mastectomy (AHR, 5.13; 95% CI, 1.87-14.08) or neurosurgery (AHR, 2.47; 95% CI, 1.09-5.61) (compared with orthopedic surgery), and body mass index (AHR, 1.05; 95% CI, 1.01-1.08 per unit increase) were independently associated with S aureus SSIs and BSIs.CONCLUSIONS AND RELEVANCE: In this cohort study of surgical patients, S aureus carriage was associated with an increased risk of developing S aureus SSIs and BSIs. Both modifiable and nonmodifiable etiologic factors were associated with this risk and should be addressed in those at increased S aureus SSI and BSI risk.",

keywords = "Aged, Female, Humans, Male, Breast Neoplasms/complications, Cohort Studies, Mastectomy, Staphylococcal Infections/prevention & control, Staphylococcus aureus, Surgical Wound Infection/prevention & control, Middle Aged",

author = "{ASPIRE-SSI Study Team} and Troeman, {Darren P R} and Derek Hazard and Leen Timbermont and Surbhi Malhotra-Kumar and {van Werkhoven}, {Cornelis H} and Martin Wolkewitz and Alexey Ruzin and Herman Goossens and Bonten, {Marc J M} and Stephan Harbarth and Frangiscos Sifakis and Kluytmans, {Jan A J W} and Jelle Vlaeminck and Tuba Vilken and Xavier, {Basil Britto} and Christine Lammens and {van Esschoten}, Marjolein and Paling, {Fleur P} and Claudia Recanatini and Frank Coenjaerts and Bret Sellman and Christine Tkaczyk and Susanne Weber and Ekkelenkamp, {Miquel Bart} and {van der Laan}, Lijckle and Vierhout, {Bastiaan P} and Elodie Couv{\'e}-Deacon and Miruna David and David Chadwick and Llewelyn, {Martin J} and Andrew Ustianowski and Antony Bateman and Damian Mawer and Biljana Carevic and Sonja Konstantinovic and Zorana Djordjevic and {Del Toro-L{\'o}pez}, {Mar{\'i}a Dolores} and Gallego, {Juan Pablo Horcajada} and Dolores Escudero and Rojo, {Miquel Pujol} and Julian Torre-Cisneros and Francesco Castelli and Giuseppe Nardi and Pamela Barbadoro and Mait Altmets and Piret Mitt and Adrian Todor and Serban-Ion Bubenek-Turconi and Dan Corneci and Dorel Sandesc",

year = "2023",

month = oct,

day = "2",

doi = "10.1001/jamanetworkopen.2023.39793",

language = "English",

volume = "6",

pages = "e2339793",

journal = "Jama network open",

issn = "2574-3805",

publisher = "AMER MEDICAL ASSOC",

number = "10",

}

ASPIRE-SSI Study Team, Troeman, DPR, Hazard, D, Timbermont, L, Malhotra-Kumar, S, van Werkhoven, CH, Wolkewitz, M, Ruzin, A, Goossens, H, Bonten, MJM, Harbarth, S, Sifakis, F & Kluytmans, JAJW 2023, 'Postoperative Staphylococcus aureus Infections in Patients With and Without Preoperative Colonization', Jama network open, vol. 6, no. 10, pp. e2339793. https://doi.org/10.1001/jamanetworkopen.2023.39793

TY - JOUR

T1 - Postoperative Staphylococcus aureus Infections in Patients With and Without Preoperative Colonization

AU - ASPIRE-SSI Study Team

AU - Troeman, Darren P R

AU - Hazard, Derek

AU - Timbermont, Leen

AU - Malhotra-Kumar, Surbhi

AU - van Werkhoven, Cornelis H

AU - Wolkewitz, Martin

AU - Ruzin, Alexey

AU - Goossens, Herman

AU - Bonten, Marc J M

AU - Harbarth, Stephan

AU - Sifakis, Frangiscos

AU - Kluytmans, Jan A J W

AU - Vlaeminck, Jelle

AU - Vilken, Tuba

AU - Xavier, Basil Britto

AU - Lammens, Christine

AU - van Esschoten, Marjolein

AU - Paling, Fleur P

AU - Recanatini, Claudia

AU - Coenjaerts, Frank

AU - Sellman, Bret

AU - Tkaczyk, Christine

AU - Weber, Susanne

AU - Ekkelenkamp, Miquel Bart

AU - van der Laan, Lijckle

AU - Vierhout, Bastiaan P

AU - Couvé-Deacon, Elodie

AU - David, Miruna

AU - Chadwick, David

AU - Llewelyn, Martin J

AU - Ustianowski, Andrew

AU - Bateman, Antony

AU - Mawer, Damian

AU - Carevic, Biljana

AU - Konstantinovic, Sonja

AU - Djordjevic, Zorana

AU - Del Toro-López, María Dolores

AU - Gallego, Juan Pablo Horcajada

AU - Escudero, Dolores

AU - Rojo, Miquel Pujol

AU - Torre-Cisneros, Julian

AU - Castelli, Francesco

AU - Nardi, Giuseppe

AU - Barbadoro, Pamela

AU - Altmets, Mait

AU - Mitt, Piret

AU - Todor, Adrian

AU - Bubenek-Turconi, Serban-Ion

AU - Corneci, Dan

AU - Sandesc, Dorel

PY - 2023/10/2

Y1 - 2023/10/2

N2 - IMPORTANCE: Staphylococcus aureus surgical site infections (SSIs) and bloodstream infections (BSIs) are important complications of surgical procedures for which prevention remains suboptimal. Contemporary data on the incidence of and etiologic factors for these infections are needed to support the development of improved preventive strategies.OBJECTIVES: To assess the occurrence of postoperative S aureus SSIs and BSIs and quantify its association with patient-related and contextual factors.DESIGN, SETTING, AND PARTICIPANTS: This multicenter cohort study assessed surgical patients at 33 hospitals in 10 European countries who were recruited between December 16, 2016, and September 30, 2019 (follow-up through December 30, 2019). Enrolled patients were actively followed up for up to 90 days after surgery to assess the occurrence of S aureus SSIs and BSIs. Data analysis was performed between November 20, 2020, and April 21, 2022. All patients were 18 years or older and had undergone 11 different types of surgical procedures. They were screened for S aureus colonization in the nose, throat, and perineum within 30 days before surgery (source population). Both S aureus carriers and noncarriers were subsequently enrolled in a 2:1 ratio.EXPOSURE: Preoperative S aureus colonization.MAIN OUTCOMES AND MEASURES: The main outcome was cumulative incidence of S aureus SSIs and BSIs estimated for the source population, using weighted incidence calculation. The independent association of candidate variables was estimated using multivariable Cox proportional hazards regression models.RESULTS: In total, 5004 patients (median [IQR] age, 66 [56-72] years; 2510 [50.2%] female) were enrolled in the study cohort; 3369 (67.3%) were S aureus carriers. One hundred patients developed S aureus SSIs or BSIs within 90 days after surgery. The weighted cumulative incidence of S aureus SSIs or BSIs was 2.55% (95% CI, 2.05%-3.12%) for carriers and 0.52% (95% CI, 0.22%-0.91%) for noncarriers. Preoperative S aureus colonization (adjusted hazard ratio [AHR], 4.38; 95% CI, 2.19-8.76), having nonremovable implants (AHR, 2.00; 95% CI, 1.15-3.49), undergoing mastectomy (AHR, 5.13; 95% CI, 1.87-14.08) or neurosurgery (AHR, 2.47; 95% CI, 1.09-5.61) (compared with orthopedic surgery), and body mass index (AHR, 1.05; 95% CI, 1.01-1.08 per unit increase) were independently associated with S aureus SSIs and BSIs.CONCLUSIONS AND RELEVANCE: In this cohort study of surgical patients, S aureus carriage was associated with an increased risk of developing S aureus SSIs and BSIs. Both modifiable and nonmodifiable etiologic factors were associated with this risk and should be addressed in those at increased S aureus SSI and BSI risk.

AB - IMPORTANCE: Staphylococcus aureus surgical site infections (SSIs) and bloodstream infections (BSIs) are important complications of surgical procedures for which prevention remains suboptimal. Contemporary data on the incidence of and etiologic factors for these infections are needed to support the development of improved preventive strategies.OBJECTIVES: To assess the occurrence of postoperative S aureus SSIs and BSIs and quantify its association with patient-related and contextual factors.DESIGN, SETTING, AND PARTICIPANTS: This multicenter cohort study assessed surgical patients at 33 hospitals in 10 European countries who were recruited between December 16, 2016, and September 30, 2019 (follow-up through December 30, 2019). Enrolled patients were actively followed up for up to 90 days after surgery to assess the occurrence of S aureus SSIs and BSIs. Data analysis was performed between November 20, 2020, and April 21, 2022. All patients were 18 years or older and had undergone 11 different types of surgical procedures. They were screened for S aureus colonization in the nose, throat, and perineum within 30 days before surgery (source population). Both S aureus carriers and noncarriers were subsequently enrolled in a 2:1 ratio.EXPOSURE: Preoperative S aureus colonization.MAIN OUTCOMES AND MEASURES: The main outcome was cumulative incidence of S aureus SSIs and BSIs estimated for the source population, using weighted incidence calculation. The independent association of candidate variables was estimated using multivariable Cox proportional hazards regression models.RESULTS: In total, 5004 patients (median [IQR] age, 66 [56-72] years; 2510 [50.2%] female) were enrolled in the study cohort; 3369 (67.3%) were S aureus carriers. One hundred patients developed S aureus SSIs or BSIs within 90 days after surgery. The weighted cumulative incidence of S aureus SSIs or BSIs was 2.55% (95% CI, 2.05%-3.12%) for carriers and 0.52% (95% CI, 0.22%-0.91%) for noncarriers. Preoperative S aureus colonization (adjusted hazard ratio [AHR], 4.38; 95% CI, 2.19-8.76), having nonremovable implants (AHR, 2.00; 95% CI, 1.15-3.49), undergoing mastectomy (AHR, 5.13; 95% CI, 1.87-14.08) or neurosurgery (AHR, 2.47; 95% CI, 1.09-5.61) (compared with orthopedic surgery), and body mass index (AHR, 1.05; 95% CI, 1.01-1.08 per unit increase) were independently associated with S aureus SSIs and BSIs.CONCLUSIONS AND RELEVANCE: In this cohort study of surgical patients, S aureus carriage was associated with an increased risk of developing S aureus SSIs and BSIs. Both modifiable and nonmodifiable etiologic factors were associated with this risk and should be addressed in those at increased S aureus SSI and BSI risk.

KW - Aged

KW - Female

KW - Humans

KW - Male

KW - Breast Neoplasms/complications

KW - Cohort Studies

KW - Mastectomy

KW - Staphylococcal Infections/prevention & control

KW - Staphylococcus aureus

KW - Surgical Wound Infection/prevention & control

KW - Middle Aged

U2 - 10.1001/jamanetworkopen.2023.39793

DO - 10.1001/jamanetworkopen.2023.39793

M3 - Article

C2 - 37906196

SN - 2574-3805

VL - 6

SP - e2339793

JO - Jama network open

JF - Jama network open

IS - 10

ER -

Postoperative Staphylococcus aureus Infections in Patients With and Without Preoperative Colonization

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