Cutibacterium acnes is an intracellular and intra-articular commensal of the human shoulder joint

Abstract

Background: Cutibacterium acnes (C acnes) is a mysterious member of the shoulder microbiome and is associated with chronic postoperative complications and low-grade infections. Nevertheless, it is unclear whether it represents a contaminant or whether it accounts for true infections. Because it can persist intracellularly in macrophages at several body sites, it might in fact be an intra-articular commensal of the shoulder joint. Methods: In 23 consecutive, otherwise healthy patients (17 male, 6 female; 58 years) who had no previous injections, multiple specimens were taken from the intra-articular tissue during first-time arthroscopic and open shoulder surgery. The samples were investigated by cultivation, genetic phylotyping, and immunohistochemistry using C acnes-specific antibodies and confocal laser scanning microscopy. Results: In 10 patients (43.5%), cultures were C acnes-positive. Phylotype IA1 dominated the subcutaneous samples (71%), whereas type II dominated the deep tissue samples (57%). Sixteen of 23 patients (69.6%) were C acnes-positive by immunohistochemistry; in total, 25 of 40 samples were positive (62.5%). Overall, 56.3% of glenohumeral immunohistochemical samples, 62.5% of subacromial samples, and 75% of acromioclavicular (AC) joint samples were positive. In 62.5% of the tested patients, C acnes was detected immunohistochemically to reside intracellularly within stromal cells and macrophages. Discussion: These data indicate that C acnes is a commensal of the human shoulder joint, where it persists within macrophages and stromal cells. Compared with culture-based methods, immunohistochemical staining can increase C acnes detection. Phylotype II seems to be most prevalent in the deep shoulder tissue. The high detection rate of C acnes in osteoarthritic AC joints might link its intra-articular presence to the initiation of osteoarthritis.

Deciphering the low abundance microbiota of presumed aseptic hip and knee implants

“…acnes detection is increasing as evidence of its presence in presumed aseptic joints grows; for example, a recent report highlighted the presence of C . acnes in macrophages and stromal cells in shoulder joints requiring primary arthroplasty for osteoarthritis [ 48 ].…”

“…Another promising strategy is a genus-/group-specific real-time PCR panel that targets bacteria typically associated with PJI [47]. The importance of robust methods for C. acnes detection is increasing as evidence of its presence in presumed aseptic joints grows; for example, a recent report highlighted the presence of C. acnes in macrophages and stromal cells in shoulder joints requiring primary arthroplasty for osteoarthritis [48].…”

Diagnosis of orthopaedic-implant-associated infections caused by slow-growing Gram-positive anaerobic bacteria – a clinical perspective

“…Persistent or increasing pain from an area with an orthopaedic implant and joint stiffness in specific relation to PJI are the most common clinical symptoms reported in SGAB IAI. However, such symptoms are also frequently present in cases of aseptic failure (Renz et al, 2018a;Rienmuller and Borens, 2016;Jacobs et al, 2016;Wang et al, 2013;Hsu et al, 2018). The classical clinical features of IAI include fever, local signs of inflammation such as redness or warmth, pain and swelling, and a sinus tract.…”

“…Fever and local signs of inflammation are not just non-specific but also observed less frequently in SGAB IAI than pain and joint stiffness (Rieber et al, 2016;Rieber et al, 2019;Corona et al, 2014;Maroto Piñeiro et al, 2021;Randall et al, 2020;. The frequency of a sinus tract in SGAB IAI has been reported anywhere from less than 1 % up to 20 % (Renz et al, 2018a;Rienmuller and Borens, 2016;Dodson et al, 2010;Jacobs et al, 2016).…”

Genomic Analysis of Cutibacterium acnes Strains Isolated from Prosthetic Joint Infections

“…However, there is an ongoing debate if a C. acnes -positive culture obtained from a clinical specimen (always) indicates a true infection with this bacterium; there is a risk of skin-derived contamination during surgery and/or specimen handling and procession that could result in the cultivation of skin-resident C. acnes [ 14 , 15 , 16 ]. Moreover, in one study C. acnes was detected as a commensal of the native shoulder microbiome [ 17 ]. One possibility to distinguish between true infection, benign commensalism and contamination is to investigate the bacterial isolates by molecular methods, such as whole genome sequencing (WGS), in order to potentially demarcate PJI-associated types of C. acnes from types that are associated with disease-free sites.…”