Tuesday, November 22, 2022

Should surgeons doubt the value of cultures in shoulder surgery?

It is well recognized that bacterial infections are important causes of failed shoulder arthroplasy, failed cuff repairs and failed fracture fixation. The organisms most commonly responsible for these infections (Cutibacterium and coagulase negative staphylococcus (CNS)) are also found on and in healthy skin of healthy individuals as well as in the environment.

Of note, these organisms can be isolated from sterile swabs and sponges that are exposed to the air in the operating room, suggesting that specimens can be contaminated by air-borne organisms, specimen handling or microbiology laboratory processing. Knowing the results of control environmental non-clinical cultures for a surgeon's operating room is important to the interpretation of the results of clinical cultures isolated from deep tissue specimens and explants obtained at the time of revision surgery.

Between-hospital variability in the results of sterile cultures is demonstrated by the reported rates of control samples that are positive for Cutibacterium which range from 4% to 9% to 15% to 20%:

In Efficacy of topical benzoyl peroxide on the reduction of Propionibacterium acnes during shoulder surgery  4% (2 of 50) of sterile control specimens were positive for P. acnes (Cutibacterium)

In The Incidence of Propionibacterium acnes in Open Shoulder Surgery: A Controlled Diagnostic Study seven (13.0%) of fifty-four sterile control specimens returned positive for culture growth. Five of these (9%) grew P. acnes (Cutibacterium), while two (4%) grew coagulase-negative S. aureus.

In Cutibacterium acnes is Isolated from Air Swabs: Time to Doubt the Value of Traditional Cultures in Shoulder Surgery? Cutibacterium was identified by culture of sterile control swabs in 6 of 40 cases (15%) swabs and coagulase negative staphylococcus (CNS) was identified in 3 of 40 (7.5%). 

In Preoperative doxycycline does not decolonize Propionibacterium acnes from the skin of the shoulder: a randomized controlled trial 20 sterile control specimens were submitted for culture, four of which (20%) grew P. acnes (Cutibacterium).

This five fold difference among hospitals in the rate of positive cultures for sterile control specimens suggests different risks of specimen contamination in the operating room, during specimen handling and/or in the microbiological laboratory.

The magnitude of contamination from these environmental sources would be expected to be small in comparison to the load of bacteria in an infected shoulder. The authors of Characterizing the Propionibacterium Load in Revision Shoulder Arthroplasty pointed to the value of assessing the amount of bacteria in a sample using a semi-quantitative report rather than simply referring to a culture result as "positive" or "negative". In 137 Cutibacterium culture-positive revision shoulder arthroplasties the culture results were characterized by a specimen Cutibacterium value (SpCV): 0 = no growth, 0.1 = broth only or one colony only, 1 = growth on one plate quadrant, 2 = growth on two plate quadrants, 3 = growth on three plate quadrants and 4 = growth on all 4 of the plate quadrants after standard microbiological plate streaking.




The authors of Preoperative Skin-Surface Cultures Can Help to Predict the Presence of Propionibacterium in Shoulder Arthroplasty Wounds used this semi-quantitative approach to report the results of cultures for sterile control swabs submitted from the operating room in 50 cases. While 2 of the control samples had positive cultures for Cutibacterium (4%), neither (0%) of the positive control samples had a SpCV of 1 or more, indicating a very low level of contamination.

Some authors have proposed that Next Generation Squencing (NGS) may be superior to cultures in detecting bacteria doing harm in shoulders. See for example, Revision shoulder arthroplasty - what is the role of next-generation sequencing?. NGS is very sensitive to the presence of bacterial RNA and DNA. In the referenced study, NGS found evidence of no fewer than 71 different organisms in specimens from cases of revision arthroplasty. including A calcoaceticus, A excentricus, A ferrireducens, A junii, A radioresistens, A rhizogenes, A tetradius, B aggregatus, B casei, B cepacia, B dorei, B fragilis, B fungorum, B mycoides, B nordii, B thermosphacta, B thetaiotaomicron, B virosa, C tuberculostearicum, C circulans, C acidisoli, C aurimucosum, C chromoreductans, C diptheriae, C hominis, C hveragerdense, C kroppenstedtii, C paradoxus, C quinii, C striatum, C testosteroni, C tuberculostearicum, C vibrioides, C xerosis, C. acnes, E coli, E hormaechei, G ruanii, K rosea, K oxytoca, K palustris, K pneumoniae L agilis, L albida L crispatus, L manihotivorans, M catarrhalis, M granosa, M luteus, P aeruginosa P agglomerans, P saccharophilia, R gnavus, R insidiosa, R picettii, S agalactiae, S aureus (MRSA) S aureus, S cohnii S condimenti, S epidermidis S hominis, S maltophilia, S melonis, S mitis, S parasanguinis, S pettenkoferi, S piscifermentans, and S sanguinis. It is not known if these results actually reflect living bacteria in the shoulder and what implications these NGS results have for treatment.

The authors of Cutibacterium acnes is Isolated from Air Swabs: Time to Doubt the Value of Traditional Cultures in Shoulder Surgery? suggest that NGS is capable of identifying pathogens and the relative percent abundance in which they appear within a sample. They state, "due to budgetary limitations and the cost of NGS, our sample size was admittedly small and only included one sample for culture and NGS from each case".

For 40 consecutive cases they opened and exposed sterile swabs to the air in the operating room for 5 seconds.  One swab was sent to their microbiology laboratory for aerobic and anaerobic culture and held for 13 days. The other sample was sent for NGS, where samples were amplified for pyrosequencing using a forward and reverse fusion primer and matched against a DNA library for species identification.

Cutibacterium was identified by culture in 6/40 (15%) swabs and coagulase negative staphylococcus (CNS) was identified in 3/40 (7.5%). When considering the semi-quantitative assessment of bacterial growth, all six samples with isolated Cutibacterium were rated as very light growth, a finding consistent with the very low SpCVs in the two positive control cultures in Preoperative Skin-Surface Cultures Can Help to Predict the Presence of Propionibacterium in Shoulder Arthroplasty Wounds . 

2/40 cases (5%) had positive NGS sequencing with polymicrobial results in the distributions shown below.

Case #6: 
P. aeruginosa (26%), P. melaninogenica (19%),  C. tuscaniense (12%),  S. mitis (9%), B. japonicum (8%), A. wolffii (7%), C. appendicis (4%), B. antiquum (4%), A. schindleri (2%)

Case #20: S. hominis (31%), S. epidermidis (24%), M. subterranean (11%), C. kroppenstedtii (8%), E. biforme (8%), P. submarinus (4%), N. oleivorans (3%), Cutibacterium (3%)

Comment: From the foregoing, it can be concluded that
(1) contamination of sterile swabs can occur between the time of opening of the swab and the final analysis of bacterial cultures by the microbiology lab. The resulting positive cultures are not "false positives" but rather positive cultures resulting from contamination
(2) the rate of contamination from the operating room environment, specimen transport and laboratory procedures varies widely among medical centers
(3) the bacterial load - as reflected by the specimen Cutibacterium value  (SpCV) -  in contaminated sterile swabs is small in comparison to the SpCV typically seen in cultures of deep tissues and explants retrieved from shoulders with periprosthetic infections; thus reporting the culture results using a  semiquantitative system to reflect bacterial load helps identify clinically important positive cultures.
(4) Next Generation Sequencing is an expensive test that reveals RNA and DNA associated with a wide range of bacterial species, the preponderance of which have not been demonstrated to be pathogenetic. Thus the value of NGS in guiding therapy in shoulders with suspected infection remains to be demonstrated.
(5) In the absence of a better alternative, surgeons should continue to use bacterial cultures (assessed for bacterial load) to help guide the management of failed shoulder surgeries potentially caused by infection.


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Here are some videos that are of shoulder interest
Shoulder arthritis - what you need to know (see this link).
How to x-ray the shoulder (see this link).
The ream and run procedure (see this link).
The total shoulder arthroplasty (see this link).
The cuff tear arthropathy arthroplasty (see this link).
The reverse total shoulder arthroplasty (see this link).
The smooth and move procedure for irreparable rotator cuff tears (see this link).
Shoulder rehabilitation exercises (see this link).