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Investigation of synovial fluid induced Staphylococcus aureus aggregate development and its impact on surface attachment and biofilm formation

Investigation of synovial fluid induced Staphylococcus aureus aggregate development and its impact on surface attachment and biofilm formation
Investigation of synovial fluid induced Staphylococcus aureus aggregate development and its impact on surface attachment and biofilm formation
Periprosthetic joint infections (PJIs) are a devastating complication that occurs in 2% of patients following joint replacement. These infections are costly and difficult to treat, often requiring multiple corrective surgeries and prolonged antimicrobial treatments. The Gram-positive bacterium Staphylococcus aureus is one of the most common causes of PJIs, and it is often resistant to a number of commonly used antimicrobials. This tolerance can be partially attributed to the ability of S. aureus to form biofilms. Biofilms associated with the surface of indwelling medical devices have been observed on components removed during chronic infection, however, the development and localization of biofilms during PJIs remains unclear. Prior studies have demonstrated that synovial fluid, in the joint cavity, promotes the development of bacterial aggregates with many biofilm-like properties, including antibiotic resistance. We anticipate these aggregates have an important role in biofilm formation and antibiotic tolerance during PJIs. Therefore, we sought to determine specifically how synovial fluid promotes aggregate formation and the impact of this process on surface attachment. Using flow cytometry and microscopy, we quantified the aggregation of various clinical S. aureus strains following exposure to purified synovial fluid components. We determined that fibrinogen and fibronectin promoted bacterial aggregation, while cell free DNA, serum albumin, and hyaluronic acid had minimal effect. To determine how synovial fluid mediated aggregation affects surface attachment, we utilized microscopy to measure bacterial attachment. Surprisingly, we found that synovial fluid significantly impeded bacterial surface attachment to a variety of materials. We conclude from this study that fibrinogen and fibronectin in synovial fluid have a crucial role in promoting bacterial aggregation and inhibiting surface adhesion during PJI. Collectively, we propose that synovial fluid may have conflicting protective roles for the host by preventing adhesion to surfaces, but by promoting bacterial aggregation is also contributing to the development of antibiotic tolerance.

Staphylococcus aureus aggregate development, biofilm formation, surface attachment, synovial fluid
1932-6203
Pestrak, Matthew J.
201ceea9-9ad8-42d5-867b-91565b139327
Gupta, Tripti Thapa
81131501-352a-489d-bffe-8910035598f5
Dusane, Devendra H.
9a47c5eb-5587-4f1d-bfd4-8548681be2bc
Guzior, Doug V.
484f5493-1738-45ea-8602-1a3f8b28f1e7
Staats, Amelia
ddd60847-7abf-43c1-a933-60b1abcec2bb
Harro, Jan
a705f926-3a28-497e-ac54-5243087f3da8
Horswill, Alexander R.
7590c3a8-9933-4300-abed-e1b94faafaa6
Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f
Pestrak, Matthew J.
201ceea9-9ad8-42d5-867b-91565b139327
Gupta, Tripti Thapa
81131501-352a-489d-bffe-8910035598f5
Dusane, Devendra H.
9a47c5eb-5587-4f1d-bfd4-8548681be2bc
Guzior, Doug V.
484f5493-1738-45ea-8602-1a3f8b28f1e7
Staats, Amelia
ddd60847-7abf-43c1-a933-60b1abcec2bb
Harro, Jan
a705f926-3a28-497e-ac54-5243087f3da8
Horswill, Alexander R.
7590c3a8-9933-4300-abed-e1b94faafaa6
Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f

Pestrak, Matthew J., Gupta, Tripti Thapa, Dusane, Devendra H., Guzior, Doug V., Staats, Amelia, Harro, Jan, Horswill, Alexander R. and Stoodley, Paul (2020) Investigation of synovial fluid induced Staphylococcus aureus aggregate development and its impact on surface attachment and biofilm formation. PLoS ONE, 15 (4), [e0231791]. (doi:10.1371/journal.pone.0231791).

Record type: Article

Abstract

Periprosthetic joint infections (PJIs) are a devastating complication that occurs in 2% of patients following joint replacement. These infections are costly and difficult to treat, often requiring multiple corrective surgeries and prolonged antimicrobial treatments. The Gram-positive bacterium Staphylococcus aureus is one of the most common causes of PJIs, and it is often resistant to a number of commonly used antimicrobials. This tolerance can be partially attributed to the ability of S. aureus to form biofilms. Biofilms associated with the surface of indwelling medical devices have been observed on components removed during chronic infection, however, the development and localization of biofilms during PJIs remains unclear. Prior studies have demonstrated that synovial fluid, in the joint cavity, promotes the development of bacterial aggregates with many biofilm-like properties, including antibiotic resistance. We anticipate these aggregates have an important role in biofilm formation and antibiotic tolerance during PJIs. Therefore, we sought to determine specifically how synovial fluid promotes aggregate formation and the impact of this process on surface attachment. Using flow cytometry and microscopy, we quantified the aggregation of various clinical S. aureus strains following exposure to purified synovial fluid components. We determined that fibrinogen and fibronectin promoted bacterial aggregation, while cell free DNA, serum albumin, and hyaluronic acid had minimal effect. To determine how synovial fluid mediated aggregation affects surface attachment, we utilized microscopy to measure bacterial attachment. Surprisingly, we found that synovial fluid significantly impeded bacterial surface attachment to a variety of materials. We conclude from this study that fibrinogen and fibronectin in synovial fluid have a crucial role in promoting bacterial aggregation and inhibiting surface adhesion during PJI. Collectively, we propose that synovial fluid may have conflicting protective roles for the host by preventing adhesion to surfaces, but by promoting bacterial aggregation is also contributing to the development of antibiotic tolerance.

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Accepted/In Press date: 31 March 2020
e-pub ahead of print date: 17 April 2020
Keywords: Staphylococcus aureus aggregate development, biofilm formation, surface attachment, synovial fluid

Identifiers

Local EPrints ID: 439454
URI: http://eprints.soton.ac.uk/id/eprint/439454
ISSN: 1932-6203
PURE UUID: f14fb0fe-39ad-4b25-b1a3-66082caa735d
ORCID for Paul Stoodley: ORCID iD orcid.org/0000-0001-6069-273X

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Date deposited: 23 Apr 2020 16:36
Last modified: 28 Apr 2022 02:02

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Contributors

Author: Matthew J. Pestrak
Author: Tripti Thapa Gupta
Author: Devendra H. Dusane
Author: Doug V. Guzior
Author: Amelia Staats
Author: Jan Harro
Author: Alexander R. Horswill
Author: Paul Stoodley ORCID iD

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