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Detection of Cutibacterium acnes in Tissue Samples from Clean Primary Shoulder Surgeries – Part II

Abstract

Objective

Research and identification of Cutibacterium acnes (C. acnes) and other microorganisms in deeptissue samples collected in clean shoulder surgeries of patients who did not undergo any previous invasive joint procedure and who had no clinical history of infection.

Methods

We analyzed the results of cultures of intraoperative deep tissue samples from 84 patients submitted to primary clean shoulder surgery. Tubes containing culture medium were used for storage and transport of anaerobic agents, prolonged incubation time, and mass spectrometer for diagnosis of bacterial agents.

Results

Bacteria growth was evidenced in 34 patients (40.4%) of the 84 included in the study. Of these, 23 had growth of C. acnes in at least one sample of deep tissue collected, corresponding to 27.3% of the total patients. The second most common agent was Staphylococcus epidermidis, present in 7.2% of the total individuals included. We showed a higher relationship between sample positivity and males, a lower mean age, absence of diabetes mellitus, ASA I score, and antibiotic prophylaxis in anesthetic induction with cefuroxime.

Conclusions

A high percentage of isolates of different bacteria was found in shoulder tissue samples of patients undergoing clean and primary surgeries, who had no history of previous infection. Identification of C. acnes was high (27.6%), and Staphylococcus epidermidis was the second most frequent agent (7.2%).

Keywords
Cutibacterium acnes ; gram-positive bacterial infections; Staphylococcus epidermidis ; shoulder

Resumo

Objetivo

Pesquisa e identificação de Cutibacterium acnes (C. acnes) e de outros microrganismos em amostras de tecidos profundos coletados em cirurgias limpas de ombro em pacientes que não foram submetidos a nenhum procedimento invasivo articular prévio e que não possuíam antecedentes clínicos de infecção.

Métodos

Foram analisados os resultados das culturas de amostras de tecidos profundos intraoperatórias de 84 pacientes submetidos à cirurgia limpa primária do ombro. Foram utilizados tubos contendo meio de cultivo para armazenamento e transporte de agentes anaeróbicos, tempo prolongado de incubação e espectrômetro de massa para diagnósticos de agentes bacterianos.

Resultados

Foi evidenciado o crescimento de bactérias em 34 pacientes (40,4%) dos 84 incluídos no estudo. Desses, 23 apresentavam crescimento de C. acnes em pelo menos uma amostra de tecido profundo coletada, correspondendo a 27,3% do total de pacientes. O segundo agente mais encontrado foi o Staphylococcus epidermidis, presente em 7,2% do total de indivíduos incluídos. Evidenciamos maior relação da positividade de amostras com o gênero masculino, uma média de idade inferior, a ausência de diabetes mellitus, o escore ASA I e a profilaxia antibiótica na indução anestésica com cefuroxima.

Conclusões

Verificou-se um elevado percentual de isolados de diferentes bactérias em amostras de tecidos de ombros de pacientes submetidos a cirurgias limpas e primárias e sem histórico de infecção anterior. A identificação de C. acnes foi elevada (27,6%) e o Staphylococcus epidermidis foi o segundo agente mais frequente (7,2%).

Palavras-chave
Cutibacterium acnes; infecções por bactérias gram-positivas; ombro; Staphylococcus epidermidis

Introduction

Cutibacterium acnes (C. acnes), formerly called Propionibacterium acnes, is a gram-positive, lipophilic, nonsporulate, and slow-growing anaerobic bacterial agent.11 Achermann Y, Goldstein EJ, Coenye T, Shirtliff ME. Propionibacterium acnes: from commensal to opportunistic biofilm-associated implant pathogen. Clin Microbiol Rev 2014;27(03): 419–440 It is a human skin commensal species present in regions with sebaceous follicles, especially in males.22 Patel A, Calfee RP, Plante M, Fischer SA, Green A. Propionibacterium acnes colonization of the human shoulder. J Shoulder Elbow Surg 2009;18(06):897–902, 33 Levy PY, Fenollar F, Stein A, et al. Propionibacterium acnes postoperative shoulder arthritis: an emerging clinical entity. Clin Infect Dis 2008;46(12):1884–1886 Although it can be found in the hip and knee, its presence is more notorious in the shoulder.22 Patel A, Calfee RP, Plante M, Fischer SA, Green A. Propionibacterium acnes colonization of the human shoulder. J Shoulder Elbow Surg 2009;18(06):897–902, 33 Levy PY, Fenollar F, Stein A, et al. Propionibacterium acnes postoperative shoulder arthritis: an emerging clinical entity. Clin Infect Dis 2008;46(12):1884–1886 In patients submitted for the first time to shoulder surgery, without previous clinical signs and symptoms of infection, the presence of C. acnes is verified in up to 41.8% of deep tissue samples.44 Hudek R, Sommer F, Kerwat M, Abdelkawi AF, Loos F, Gohlke F. Propionibacterium acnes in shoulder surgery: true infection, contamination, or commensal of the deep tissue? J Shoulder Elbow Surg 2014;23(12):1763–1771

Laboratory diagnosis of C. acnes is challenging. Bacteriological cultures require specific care to avoid false-negative results or doubts between infection and contamination of samples.55 Boisrenoult P. Cutibacterium acnes prosthetic joint infection: Diagnosis and treatment. Orthop Traumatol Surg Res 2018;104 (1S):S19–S24 Rapid transport from sample collection to laboratory should promote survival for anaerobic agents. Furthermore, the incubation period in an anaerobic environment must be prolonged for at least 14 days to allow slow bacterial growth and its isolation.66 Schäfer P, Fink B, Sandow D, Margull A, Berger I, Frommelt L. Prolonged bacterial culture to identify late periprosthetic joint infection: a promising strategy. Clin Infect Dis 2008;47(11): 1403–1409 Faced with so many difficulties in the diagnosis of growth in culture medium, previous studies argue that there is a large number of underdiagnoses of C. acnes colonization.66 Schäfer P, Fink B, Sandow D, Margull A, Berger I, Frommelt L. Prolonged bacterial culture to identify late periprosthetic joint infection: a promising strategy. Clin Infect Dis 2008;47(11): 1403–1409 In a previous study published by the same group, it was evidenced that tissue samples collected and transported in a dry vial and incubated for up to 7 days presented a 99.2% rate of negative results for the identification of any microorganism, alerting to the low diagnostic efficacy of laboratory investigation standards in our country.77 Miyazaki AN, Checchia CS, Fonseca Filho JM, Gonçalves GV, Conte LHG, Sella GV. Caracterização da carga bacteriana em cirurgias primárias do ombro. Rev Bras Ortop 2021 New laboratory bacteriological investigation techniques are under development to improve diagnosis, of which we highlight genetic sequencing and mass spectrometry.55 Boisrenoult P. Cutibacterium acnes prosthetic joint infection: Diagnosis and treatment. Orthop Traumatol Surg Res 2018;104 (1S):S19–S24, 88 Namdari S, Nicholson T, Abboud J, et al. Comparative study of cultures and next-generation sequencing in the diagnosis of shoulder prosthetic joint infections. J Shoulder Elbow Surg 2019;28(01):1–8, 99 Barreau M, Pagnier I, La Scola B. Improving the identification of anaerobes in the clinical microbiology laboratory through MALDI-TOF mass spectrometry. Anaerobe 2013;22:123–125

The aim of this study is to identify the presence of C. acnes and other bacterial agents in deep shoulder tissue samples of patients who have not undergone any previous invasive procedure in this joint and who did not have a clinical history of infection (clean surgeries).

Casuistic and Methods

This is a prospective, longitudinal, sequential, observational, and multicentric cohort study in patients undergoing clean and elective shoulder surgeries from July 2020 to November 2020, from whom deep tissue samples were collected sterilely for the research of microorganisms, including C. acnes. The study was approved by the Research Ethics Committee of our institution.

The results of 84 shoulder cultures collected from 84 patients submitted to primary clean surgery in eight different hospitals in the city of São Paulo were analyzed. Of these patients, 45 (54%) were male and 39 (46%) were female; ages ranged from 19 to 94 years (mean of 51.5). Regarding ethnicity, 63 individuals (75%) were white, 12 (14%) were mixed-race, 5 (6%) were Asian-American, and 4 (5%) were black. As for the surgical technique, 38 (45%) underwent arthroscopic procedure, and 46 (55%) underwent open procedure. All patients were older than 18-years-old, with no previous history of shoulder infection, and underwent primary shoulder surgery.

We correlate the comorbidities of patients with the classification of the American Society of Anesthesiologists (ASA),1010 Saklad M. Grading of patients for surgical procedures. Anesthesiol 1941;2:281–284 21 individuals (25%) were classified as ASA I, 61 (73%) as ASA II, and 2 (2.3%) as ASA III. All patients in this study received antibiotic prophylaxis, with first or second generation cephalosporins—cefazolin or cefuroxime, respectively—in anesthetic induction and for 24hours after the surgical procedure.

In each shoulder surgery, three intraoperative samples of bone (humerus head, acromion, or distal third of the clavicle), tendon (supraspinal, tendon of the long head of the biceps, or joint tendon), and subacromial pouch of about 0.5cm3, were collected for laboratory analysis of bacteria proliferation in aerobic and anaerobic cultures. Of the three deep tissue samples selected, two were collected separately in sterile vials containing thioglycolate broth and one was collected in a sterile vial with 0.9% saline solution. The vials were sealed and sent to the microbiological research laboratory (Special Laboratory of Clinical Microbiology of the Universidade Federal de São Paulo) immediately after the procedure by the surgical team members themselves.

In the laboratory, the samples in the vials containing thioglycolate (►Figure 1) were placed in the anaerobiosis jar at 37°C for 14 days. The samples in 0.9% saline were transferred to the Trypic Soy Broth (TSB) liquid medium and incubated in aerobiosis at 37°C. After 14 days, in the tubes that presented turbidity (►Figure 2), 10uL of the cloudy liquid medium were inoculated in sheep blood agar plates and incubated at 37°C for another 14 days in the anaerobiosis jar. All samples in anaerobiosis and aerobiosis that showed bacterial growth were stored in TSB with 20% glycerol and frozen at -80°C (►Figure 3).

Fig. 1
Example of a vial containing thioglycolate broth, used for incubation of the collected samples.

Fig. 2
Example of turbid thioglycolate broth after sample incubation, evidencing bacterial proliferation.

Fig. 3
Petri dish containing samples of Cutibacterium acnes cultures grown in sheep’s blood agar.

The next step consisted of the identification of bacterial agents by the matrix-assisted laser desorption ionization-time of flight (MALDI-TOF MS, MALDI Biotyper, Bruker Daltonics, Germany) according tothetechnical descriptionof Dingle et al.1111 Dingle TC, Butler-Wu SM. Maldi-tof mass spectrometry for microorganism identification. Clin Lab Med 2013;33(03):589–609 (►Figures 4 and 5).

Fig. 4
Image taken from the Flexcontrol program, used to identify bacterial agents through the specific flight time graph of each microorganism. In this example, after analyzing the defined peaks, we have the identification of Staphylococcus cohnii.

Fig. 5
Image taken from the Flexcontrol program used to identify bacterial agents through the specific flight time graph of each microorganism. In this example we have the identification of Cutibacterium acnes.

The patients were followed up in the postoperative period with face-to-face physical examinations and serial radiographs during a period of up to 10 months from the first surgery performed in a patient included in the study until treatment conclusion. In patients who presented identification of bacteria in the collected samples, blood count and blood inflammatory tests were collected serially. The evaluations of patients in the postoperative period, as well as their radiographs and laboratory tests were documented in medical records, aiming at the formation of a database for a future study of the group with longer clinical follow-up time.

For statistical analysis, we used the Fisher exact test, chisquare test, Person correlation, two-sample t-test, confidence interval, and p-value, when applicable. The level of significance adopted was 0.05 (5%).

Results

After laboratory analysis of the collected samples, the growth of bacterial agents was evidenced in 40.5% of the patients (34/84). Of these, 23 had C. acnes in at least one of the samples collected, corresponding to 27.3% of the total patients, and 67.6% of the patients presented positive samples for growth of any microorganism. There were 4 patients (4.8%) who presented more than one positive sample for C. acnes. The second most identified microbial agent was Staphylococcus epidermidis, present in 6 individuals (7.2% of the total and 18.2% of the positive ones), while the third agent was Escherichia coli, identified in 3 individuals (3.5% of the total and 8.8% of the positive). (►Table 1)

Table 1
Total number of individuals who presented bacterial identification of at least one sample, the bacterial agents identified, and the respective risk factors evidenced: age, gender, ASA, antibiotic prophylaxis and diabetes mellitus

Among the 23 individuals who had growth of C. acnes in the samples, 18 (78.3%) were male. There was a statistically significant difference for males both in those positive for C. acnes (p = 0.05) and in the total number of positives (p = 0.01). There was no statistically significant difference for ethnicity or for the surgical technique applied (open or arthroscopic surgeries).

Of the 34 individuals positive for any microorganism, 11 (32.4%) were classified as ASA I, while in individuals with no growth of microorganisms, this group corresponded to only 14% (7 among 52 individuals). Statistical significance was evidenced for this group of patients (p = 0.04). When the patients positive for C. acnes were evaluated, it was found that 8 (34.7%) were classified as ASA I, and we found no statistical significance, but a trend (p = 0.08). It was also observed that individuals with diabetes mellitus had lower isolation of bacteria, corresponding to only 3 (13%) individuals of the 23 positives for C. acnes (p = 0.04), and 6 (17.6%) of the 34 positives for any bacterium (p = 0.04).

In 8 (35%) of the individuals with samples positive for C. acnes, cefazolin was administered as a prophylactic antibiotic in anesthetic induction and during the 24 hours postoperatively. In 15 (65%) individuals, cefuroxime was administered in the same period, 5 of which presented two or more positive samples for C. acnes (83% of individuals with two or more positive samples). We showed a statistically significant difference in antibiotic therapy prophylaxis for the detection of a positive sample for C. acnes (p = 0.03) and there was no statistical significance for two or more positive samples for C. acnes, but there was a trend (p = 0.09). Among the 252 samples collected, 53 (21%) were positive for microorganism identification. Of the positive samples, 30.5% were collected in vials with saline solution and 69.8% were collected in vials containing thioglycolate. Tendon samples had 35% bacterial identification, followed by sub-acromial pouch (34%), and bone (31%) samples. Additionally, 22 patients (64.7% of the positive) presented monomicrobial results—that is, only one of the samples positive for bacterial identification—while 12 (35.3%) presented polymicrobial results—that is, two or more samples positive for the same or different agents. C. acnes was the most identified agent in patients with monomicrobial outcome (81%) and polymicrobial result (100%), and 43% of patients positive for C. acnes presented polymicrobial samples.

Discussion

The identification of potential pathogenic bacterial agents has gained emphasis in the orthopedic literature. In the study of shoulder disorders, C. acnes is highlighted as a possibly pathogenic agent during the postoperative period of open and arthroscopic surgeries. More recently, its presence in samples of primary shoulder surgeries has been evidenced.44 Hudek R, Sommer F, Kerwat M, Abdelkawi AF, Loos F, Gohlke F. Propionibacterium acnes in shoulder surgery: true infection, contamination, or commensal of the deep tissue? J Shoulder Elbow Surg 2014;23(12):1763–1771, 1212 Sethi PM, Sabetta JR, Stuek SJ, et al. Presence of Propionibacterium acnes in primary shoulder arthroscopy: results of aspiration and tissue cultures. J Shoulder Elbow Surg 2015;24(05):796–803, 1313 Levy O, Iyer S, Atoun E, et al. Propionibacterium acnes: an underestimated etiology in the pathogenesis of osteoarthritis? J Shoulder Elbow Surg 2013;22(04):505–511 In the present study, we tried to evaluate the presence of C. acnes in deep tissue samples from the shoulders of patients undergoing primary clean surgeries, with no history of previous infection.

Isolation of C. acnes is difficult. In a previous study of our group, it was evidenced that the culture medium used for anaerobic microorganisms in the collection and transport containers, as well as in the prolonged incubation time of samples, are determining factors for the identification of this bacterium in primary shoulder surgeries without history of infection.77 Miyazaki AN, Checchia CS, Fonseca Filho JM, Gonçalves GV, Conte LHG, Sella GV. Caracterização da carga bacteriana em cirurgias primárias do ombro. Rev Bras Ortop 2021 Using sterile vials for dry transport, with transport carried out by outsourced laboratories to the hospital and with incubation time of up to 7 days, we obtained only one positive sample for coagulase-negative Staphylococci among the 47 shoulders studied,77 Miyazaki AN, Checchia CS, Fonseca Filho JM, Gonçalves GV, Conte LHG, Sella GV. Caracterização da carga bacteriana em cirurgias primárias do ombro. Rev Bras Ortop 2021 constituting a result below that found in the literature.44 Hudek R, Sommer F, Kerwat M, Abdelkawi AF, Loos F, Gohlke F. Propionibacterium acnes in shoulder surgery: true infection, contamination, or commensal of the deep tissue? J Shoulder Elbow Surg 2014;23(12):1763–1771, 1212 Sethi PM, Sabetta JR, Stuek SJ, et al. Presence of Propionibacterium acnes in primary shoulder arthroscopy: results of aspiration and tissue cultures. J Shoulder Elbow Surg 2015;24(05):796–803, 1313 Levy O, Iyer S, Atoun E, et al. Propionibacterium acnes: an underestimated etiology in the pathogenesis of osteoarthritis? J Shoulder Elbow Surg 2013;22(04):505–511 We understand, therefore, that the use of a methodology involving: the storage and transport of samples in saline and thioglycolate (means of transport and culture for anaerobic agents), the rapid transport from the operating room to the laboratory, the incubation time of more than 14 days, and the identification of the agents with greater sensitivity and specificity by MALDI-TOF MS, were essential factors for the correct analysis of the shoulder’s microbiota in the present study.

Following this methodology, we obtained 40.3% of positive samples for different microorganisms, of which 67.3% were positive for C. acnes (27.6% of the sample). When comparing these values with other studies, we noted that Sethi et al.1212 Sethi PM, Sabetta JR, Stuek SJ, et al. Presence of Propionibacterium acnes in primary shoulder arthroscopy: results of aspiration and tissue cultures. J Shoulder Elbow Surg 2015;24(05):796–803 found a rate of 21.8% of positive samples for C. acnes in primary arthroscopies of the shoulder, Hudek et al.44 Hudek R, Sommer F, Kerwat M, Abdelkawi AF, Loos F, Gohlke F. Propionibacterium acnes in shoulder surgery: true infection, contamination, or commensal of the deep tissue? J Shoulder Elbow Surg 2014;23(12):1763–1771 found a rate of 36.4% in open shoulder surgeries, and Levy et al.1313 Levy O, Iyer S, Atoun E, et al. Propionibacterium acnes: an underestimated etiology in the pathogenesis of osteoarthritis? J Shoulder Elbow Surg 2013;22(04):505–511 found a rate of 41.8% in primary arthroplasties. Our study did not identify a statistically significant difference between the results of patients undergoing open or arthroscopic surgeries. The second most common agent found in our study was Staphylococcus epidermidis, present in 7.2% of the total individuals included and in 18.2% of those with bacterial growth identified in the samples. This data is in accordance with the literature.55 Boisrenoult P. Cutibacterium acnes prosthetic joint infection: Diagnosis and treatment. Orthop Traumatol Surg Res 2018;104 (1S):S19–S24 We evidenced from our study data that C. acnes plays an important role in shoulder surgeries’ postsurgical care, since it corresponds to the bacterial agent most found in primary surgeries of this joint.

Epidemiologically, we were able to establish correlations between the positivity of samples, including C. acnes, and age, gender, and presence of previous comorbidities of patients. We showed that male patients presented higher rates of positive samples for any microorganism and, more specifically, for C. acnes.

The mean age in patients with positive samples was 46.2 years; and, in those with C. acnes isolation, it was 44.7 years. Both values were lower than the means of patients without isolation.

The predominance of males in the findings of C. acnes has been previously reported by several studies.22 Patel A, Calfee RP, Plante M, Fischer SA, Green A. Propionibacterium acnes colonization of the human shoulder. J Shoulder Elbow Surg 2009;18(06):897–902, 33 Levy PY, Fenollar F, Stein A, et al. Propionibacterium acnes postoperative shoulder arthritis: an emerging clinical entity. Clin Infect Dis 2008;46(12):1884–1886, 1414 Pottinger P, Butler-WuS, Neradilek MB,et al. Prognostic factors for bacterial cultures positive for Propionibacterium acnes and other organisms in a large series of revision shoulder arthroplasties performed for stiffness, pain, or loosening. J Bone Joint Surg Am 2012;94(22):2075–2083, 1515 Kaveeshwar S, Duvall G, Jones DL, et al. Risk factors for increased shoulder Cutibacterium acnes burden. JSES Int 2020;4(03): 464–469 Kaveeshwar et al.1515 Kaveeshwar S, Duvall G, Jones DL, et al. Risk factors for increased shoulder Cutibacterium acnes burden. JSES Int 2020;4(03): 464–469 found a correlation between isolation of this agent and age lower than 40 years. The higher prevalence stake in males and young people are related to the more active production of the sebaceous glands in these individuals.1515 Kaveeshwar S, Duvall G, Jones DL, et al. Risk factors for increased shoulder Cutibacterium acnes burden. JSES Int 2020;4(03): 464–469 Finally, Nagaya et al.1616 Nagaya LH, Salles MJC, Takikawa LSC, et al. Infections after shoulder arthroplasty are correlated with higher anesthetic risk score: a case-control study in Brazil. Braz J Infect Dis 2017;21(06): 613–619 showed that patients with an anesthetic risk score higher than ASA III had a higher risk of developing infection after shoulder arthroplasty. Interestingly, in our study we found a higher correlation of microorganism isolation in ASA I patients, with a tendency to isolate C. acnes. Another important relationship we found was the lower isolation of C. acnes and other bacterial agents in patients with diabetes mellitus, which is in accordance with Kaveeshwar et al.,1515 Kaveeshwar S, Duvall G, Jones DL, et al. Risk factors for increased shoulder Cutibacterium acnes burden. JSES Int 2020;4(03): 464–469 who also did not evidence this comorbidity as a risk factor for the isolation of C. acnes.

We found that prophylactic antibiotic therapy in anesthetic induction was related to the isolation of C. acnes. Proportionally, there was greater isolation inpatients receiving cefuroxime when compared to those receiving cefazolin. The international literature demonstrates rates of reduction of more than 50% of superficial and deep infections after the administration of cephalosporins in anesthetic induction of orthopedic surgeries. Cefazolin and cefuroxime are the antibiotics of choice by the American Academy of Orthopaedic Surgeons (AAOS) for elective orthopedic surgeries, with no clear predilection for one or the other.1717 Bryson DJ, Morris DLJ, Shivji FS, Rollins KR, Snape S, Ollivere BJ. Antibiotic prophylaxis in orthopaedic surgery: difficult decisions in an era of evolving antibiotic resistance. Bone Joint J 2016;98-B (08):1014–1019 Cephalosporins, in addition to having coverage for most Staphylococcus aureus and some gram-negative organisms, have a good safety profile, a long half-life time, and an efficient penetration into the bones.1717 Bryson DJ, Morris DLJ, Shivji FS, Rollins KR, Snape S, Ollivere BJ. Antibiotic prophylaxis in orthopaedic surgery: difficult decisions in an era of evolving antibiotic resistance. Bone Joint J 2016;98-B (08):1014–1019 To our knowledge, there are no previous studies demonstrating the comparative relationship between cefazolin or cefuroxime prophylaxis in the laboratory growth rate of C. acnes.

During the follow-up of the individuals, only one patient who had the isolation of Proteus mirabilis and two others with isolation of C. acnes presented nonspecific inflammatory signs 2 weeks after surgery. All patients underwent oral antibiotic therapy and were asymptomatic, with no radiographic or laboratory alterations after follow-up of up to 10 months.

It is noteworthy that the present study is the first of its kind in Brazilian orthopedics. As a positive point, it exhibits the importance of an effective methodology for collecting and transporting intraoperative samples, as well as for identifying microorganisms by new and different microbiological techniques as a substantial factor for diagnostic success, and for improving care in combating orthopedic infections. We understand that our study shows a different perspective of bacterial research in our country, which allows the identification of possible risk factors for bacterial growth. We highlight as limiting factors of the study the infeasibility of performing a multivariate analysis of the risk factors found due to the samplesize, as well as the absence of a control group.

The observation and clinical correlation of inflammatory signs and symptoms over longer periods in individuals who obtained bacterial isolation in this study is a topic of interest of our group for a new ongoing study, which aims to contemplate the importance of the qualification and quantification of the positive samples found.

Conclusion

There was a high percentage of isolates of different bacteria in shoulder tissue samples of patients submitted to clean and primary surgeries and with no history of previous infection. Identification of C. acnes was high (27.6%), and Staphylococcus epidermidis was the second most frequent agent (7.2%).

  • Financial Support
    There was no financial support from public, commercial, or non-profit sources.
  • Multicentric study carried out in the Shoulder Surgery Group of the Department of Orthopedics and Traumatology of the Faculty of Sciences Doctors from Santa Casa of São Paulo, “Fernandinho Simonsen Pavilion” (DOT – FCMSCSP) (Director: Professor Maria Fernanda Silber Caffaro); at the German Hospital Oswaldo Cruz in São Paulo (Shoulder Surgeons Group); and at the Special Laboratory of Clinical Microbiology (LEMC) of the Discipline of Infectious Diseases, Department of Medicine, Escola Paulista de Medicina, Federal University of São Paulo (UNIFESP), São Paulo, SP, Brazil.

References

  • 1
    Achermann Y, Goldstein EJ, Coenye T, Shirtliff ME. Propionibacterium acnes: from commensal to opportunistic biofilm-associated implant pathogen. Clin Microbiol Rev 2014;27(03): 419–440
  • 2
    Patel A, Calfee RP, Plante M, Fischer SA, Green A. Propionibacterium acnes colonization of the human shoulder. J Shoulder Elbow Surg 2009;18(06):897–902
  • 3
    Levy PY, Fenollar F, Stein A, et al. Propionibacterium acnes postoperative shoulder arthritis: an emerging clinical entity. Clin Infect Dis 2008;46(12):1884–1886
  • 4
    Hudek R, Sommer F, Kerwat M, Abdelkawi AF, Loos F, Gohlke F. Propionibacterium acnes in shoulder surgery: true infection, contamination, or commensal of the deep tissue? J Shoulder Elbow Surg 2014;23(12):1763–1771
  • 5
    Boisrenoult P. Cutibacterium acnes prosthetic joint infection: Diagnosis and treatment. Orthop Traumatol Surg Res 2018;104 (1S):S19–S24
  • 6
    Schäfer P, Fink B, Sandow D, Margull A, Berger I, Frommelt L. Prolonged bacterial culture to identify late periprosthetic joint infection: a promising strategy. Clin Infect Dis 2008;47(11): 1403–1409
  • 7
    Miyazaki AN, Checchia CS, Fonseca Filho JM, Gonçalves GV, Conte LHG, Sella GV. Caracterização da carga bacteriana em cirurgias primárias do ombro. Rev Bras Ortop 2021
  • 8
    Namdari S, Nicholson T, Abboud J, et al. Comparative study of cultures and next-generation sequencing in the diagnosis of shoulder prosthetic joint infections. J Shoulder Elbow Surg 2019;28(01):1–8
  • 9
    Barreau M, Pagnier I, La Scola B. Improving the identification of anaerobes in the clinical microbiology laboratory through MALDI-TOF mass spectrometry. Anaerobe 2013;22:123–125
  • 10
    Saklad M. Grading of patients for surgical procedures. Anesthesiol 1941;2:281–284
  • 11
    Dingle TC, Butler-Wu SM. Maldi-tof mass spectrometry for microorganism identification. Clin Lab Med 2013;33(03):589–609
  • 12
    Sethi PM, Sabetta JR, Stuek SJ, et al. Presence of Propionibacterium acnes in primary shoulder arthroscopy: results of aspiration and tissue cultures. J Shoulder Elbow Surg 2015;24(05):796–803
  • 13
    Levy O, Iyer S, Atoun E, et al. Propionibacterium acnes: an underestimated etiology in the pathogenesis of osteoarthritis? J Shoulder Elbow Surg 2013;22(04):505–511
  • 14
    Pottinger P, Butler-WuS, Neradilek MB,et al. Prognostic factors for bacterial cultures positive for Propionibacterium acnes and other organisms in a large series of revision shoulder arthroplasties performed for stiffness, pain, or loosening. J Bone Joint Surg Am 2012;94(22):2075–2083
  • 15
    Kaveeshwar S, Duvall G, Jones DL, et al. Risk factors for increased shoulder Cutibacterium acnes burden. JSES Int 2020;4(03): 464–469
  • 16
    Nagaya LH, Salles MJC, Takikawa LSC, et al. Infections after shoulder arthroplasty are correlated with higher anesthetic risk score: a case-control study in Brazil. Braz J Infect Dis 2017;21(06): 613–619
  • 17
    Bryson DJ, Morris DLJ, Shivji FS, Rollins KR, Snape S, Ollivere BJ. Antibiotic prophylaxis in orthopaedic surgery: difficult decisions in an era of evolving antibiotic resistance. Bone Joint J 2016;98-B (08):1014–1019

Publication Dates

  • Publication in this collection
    11 Aug 2023
  • Date of issue
    Mar-Apr 2023

History

  • Received
    15 Sept 2021
  • Accepted
    17 Aug 2022
Sociedade Brasileira de Ortopedia e Traumatologia Al. Lorena, 427 14º andar, 01424-000 São Paulo - SP - Brasil, Tel.: 55 11 2137-5400 - São Paulo - SP - Brazil
E-mail: rbo@sbot.org.br