Prosthetic Shoulder Joint Infection by Cutibacterium acnes: Does Rifampin Improve Prognosis? A Retrospective, Multicenter, Observational Study
Abstract
:1. Introduction
2. Results
2.1. Patient Baseline and Clinical Characteristics
2.2. Microbiological Characteristics and Antimicrobial Susceptibility Patterns
2.3. Surgical and Medical Therapy
2.4. Treatment Outcomes
3. Discussion
4. Methods
4.1. Study Design, Patients, and Settings
4.2. Data Collection
4.3. Definitions
4.4. Follow-Up and Treatment Success
4.5. Microbiological Methods
4.6. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Piggott, D.A.; Higgins, Y.M.; Melia, M.T.; Ellis, B.; Carroll, K.C.; McFarland, E.G.; Auwaerter, P.G. Characteristics and Treatment Outcomes of Propionibacterium acnes Prosthetic Shoulder Infections in Adults. Open Forum Infect. Dis. 2015, 3, ofv191. [Google Scholar] [CrossRef] [Green Version]
- Lutz, M.F.; Berthelot, P.; Fresard, A.; Cazorla, C.; Carricajo, A.; Vautrin, A.C.; Fessy, M.-H.; Lucht, F. Arthroplastic and osteo-synthetic infections due to Propionibacterium acnes: A retrospective study of 52 cases, 1995–2002. Eur. J. Clin. Microbiol. Infect. Dis. 2005, 24, 739–744. [Google Scholar] [CrossRef]
- Levy, P.Y.; Fenollar, F.; Stein, A.; Borrione, F.; Cohen, E.; Lebail, B.; Raoult, D. Propionibacterium acnes post-operative shoulder arthritis: An emerging clinical entity. Clin. Infect. Dis. 2008, 46, 1884–1886. [Google Scholar] [CrossRef] [Green Version]
- Walter, G.; Vernier, M.; Pinelli, P.O.; Million, M.; Coulange, M.; Seng, P.; Stein, A. Bone and joint infections due to anaerobic bacteria: An analysis of 61 cases and review of the literature. Eur. J. Clin. Microbiol. Infect. Dis. 2014, 33, 1355–1364. [Google Scholar] [CrossRef] [PubMed]
- Achermann, Y.; Sahin, F.; Schwyzer, H.; Kolling, C.; Wüst, J.; Vogt, M. Characteristics and outcome of 16 periprosthetic shoulder joint infections. Infection 2012, 41, 613–620. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cooper, M.E.; Trivedi, N.N.; Sivasundaram, L.; Karns, M.R.; Voos, J.E.; Gillespie, R.J. Diagnosis and man-agement of periprosthetic joint infection after shoulder arthroplasty. JBJS Rev. 2019, 7, e3. [Google Scholar] [CrossRef]
- Wang, B.; Toye, B.; Desjardins, M.; Lapner, P.; Lee, C. A 7-year retrospective review from 2005 to 2011 of Propionibacterium acnes shoulder infections in Ottawa, Ontario, Canada. Diagn. Microbiol. Infect. Dis. 2013, 75, 195–199. [Google Scholar] [CrossRef] [PubMed]
- Nodzo, S.R.; Boyle, K.K.; Bhimani, S.; Duquin, T.R.; Miller, A.O.; Westrich, G.H. Propionibacterium acnes Host Inflammatory Response During Periprosthetic Infection Is Joint Specific. HSS J. 2017, 13, 159–164. [Google Scholar] [CrossRef] [PubMed]
- Kanafani, Z.A.; Pien, B.C.; Varkey, J.; Basmania, C.; Kaye, K.S.; Sexton, D.J. Postoperative Joint Infections Due to Propionibacterium Species: A Case-Control Study. Clin. Infect. Dis. 2009, 49, 1083–1085. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matsen, F.A.; Whitson, A.; Neradilek, M.B.; Pottinger, P.S.; Bertelsen, A.; Hsu, J.E. Factors predictive of Cutibacterium periprosthetic shoulder infections: A retrospective study of 342 prosthetic revisions. J. Shoulder Elb. Surg. 2020, 29, 1177–1187. [Google Scholar] [CrossRef]
- Osmon, D.R.; Berbari, E.F.; Berendt, A.R.; Lew, D.; Zimmerli, W.; Steckelberg, J.M.; Rao, N.; Hanssen, A.; Wilson, W.R. Diagnosis and management of prosthetic joint infection: Clinical practice guidelines by the infectious diseases Society of America. Clin. Infect. Dis. 2013, 56, e1–e25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tafin, U.F.; Corvec, S.; Betrisey, B.; Zimmerli, W.; Trampuz, A. Role of rifampin against Propionibacte-rium acnes biofilm in vitro and in an experimental foreign-body infection model. Antimicrob. Agents Chemother. 2012, 56, 1885–1891. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sendi, P.; Zimmerli, W. Antimicrobial treatment concepts for orthopaedic device-related infection. Clin. Microbiol. Infect. 2012, 18, 1176–1184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Butler-Wu, S.M.; Burns, E.M.; Pottinger, P.S.; Magaret, A.S.; Rakeman, J.L.; Matsen, F.A.; Cookson, B.T. Optimization of Periprosthetic Culture for Diagnosis of Propionibacterium acnes Prosthetic Joint Infection. J. Clin. Microbiol. 2011, 49, 2490–2495. [Google Scholar] [CrossRef] [Green Version]
- Frangiamore, S.J.; Saleh, A.; Grosso, M.J.; Alolabi, B.; Bauer, T.W.; Iannotti, J.P.; Ricchetti, E.T. Early versus late cul-ture growth of Propionibacterium acnes in revision shoulder arthroplasty. J. Bone Jt. Surg. Am. Vol. 2015, 97, 1149–1158. [Google Scholar] [CrossRef] [PubMed]
- Hsu, J.E.; Somerson, J.S.; Vo, K.V.; Matsen, F.A. What is a “periprosthetic shoulder infection”? A systematic review of two decades of publications. Int. Orthop. 2017, 41, 813–822. [Google Scholar] [CrossRef] [PubMed]
- Dodson, C.C.; Craig, E.V.; Cordasco, F.A.; Dines, D.M.; Dines, J.S.; DiCarlo, E.; Brause, B.D.; Warren, R.F. Propionibacterium ac-nes infection after shoulder arthroplasty: A diagnostic challenge. J. Shoulder Elb. Surg. 2010, 19, 303–307. [Google Scholar] [CrossRef] [PubMed]
- Patel, A.; Calfee, R.P.; Plante, M.; Fischer, S.A.; Green, A. Propionibacterium acnes colonization of the human shoulder. J. Shoulder Elb. Surg. 2009, 18, 897–902. [Google Scholar] [CrossRef]
- Zeller, V.; Ghorbani, A.; Strady, C.; Leonard, P.; Mamoudy, P.; Desplaces, N. Propionibacterium acnes: An agent of prosthetic joint infection and colonization. J. Infect. 2007, 55, 119–124. [Google Scholar] [CrossRef]
- Egglestone, A.; Ingoe, H.; Rees, J.; Thomas, M.; Jeavons, R.; Rangan, A. Scoping review: Diagnosis and management of periprosthetic joint infection in shoulder arthroplasty. Shoulder Elb. 2019, 11, 167–181. [Google Scholar] [CrossRef]
- Levy, O.; Iyer, S.; Atoun, E.; Peter, N.; Hous, N.; Cash, D.; Musa, F.; Narvani, A. Propionibacterium acnes: An underestimated etiology in the pathogenesis of osteoarthritis? J. Shoulder Elb. Surg. 2013, 22, 505–511. [Google Scholar] [CrossRef]
- Garrigues, G.E.; Zmistowski, B.; Cooper, A.M.; Green, A.; Abboud, J.; Beasley, J.; Belay, E.S.; Benito, N.; Cil, A.; Clark, B.; et al. Proceedings from the 2018 International Consensus Meeting on Orthopedic Infections: Management of periprosthetic shoulder infection. J. Shoulder Elb. Surg. 2019, 28, S67–S99. [Google Scholar] [CrossRef]
- Sperling, J.W.; Kozak, T.K.; Hanssen, A.D.; Cofield, R.H. Infection after Shoulder Arthroplasty. Clin. Orthop. Relat. Res. 2001, 382, 206–216. [Google Scholar] [CrossRef]
- Fink, B.; Sevelda, F. Periprosthetic Joint Infection of Shoulder Arthroplasties: Diagnostic and Treatment Options. BioMed Res. Int. 2017, 2017, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Simha, S.; Shields, E.J.; Wiater, J.M. Periprosthetic Infections of the Shoulder. JBJS Rev. 2018, 6, e6. [Google Scholar] [CrossRef] [PubMed]
- Paxton, E.S.; Green, A.; Krueger, V.S. Periprosthetic Infections of the Shoulder: Diagnosis and Management. J. Am. Acad. Orthop. Surg. 2019, 27, E935–E944. [Google Scholar] [CrossRef] [PubMed]
- Furustrand Tafin, U.; Trampuz, A.; Corvec, S. In vitro emergence of rifampicin resistance in Propionibacterium acnes and molecular characterization of mutations in the rpoB gene. J. Antimicrob. Chemother. 2013, 68, 523–528. [Google Scholar] [CrossRef] [Green Version]
- Tsukayama, D.T.; Estrada, R.; Gustilo, R.B. Infection after Total Hip Arthroplasty A Study of the Treatment of One Hundred and Six Infections. Available online: http://journals.lww.com/jbjsjournal (accessed on 7 March 2021).
- Zimmerli, W.; Trampuz, A.; Ochsner, P.E. Prosthetic-Joint Infections. N. Engl. J. Med. 2004, 351, 1645. Available online: www.nejm.org (accessed on 21 March 2021). [CrossRef] [PubMed] [Green Version]
- Trampuz, A.; Zimmerli, W. Prosthetic joint infections: Update in diagnosis and treatment. Swiss Med. Wkly. 2005, 135, 243–251. [Google Scholar]
- Jaime, E.; Mercedes, M.; Antonia, M.M.; Mar, S.-S. Diagnostico microbiológico de las infecciones osteoarticulares. Procedimientos en Microbiol Clínica Recomendaciones de la Sociedad Española Enfermedades Infecciosas y Microbiol Clínica. 2009, p. 1. Available online: http://www.seimc.org/documentos/protocolos/microbiologia (accessed on 21 March 2021).
- Marín, M.; Esteban, J.; Meseguer, M.A.; Sánchez-Somolinos, M. Diagnóstico microbiolgico de las infecciones osteoarticulares. Enferm. Infecc. Microbiol. Clin. 2010, 28, 534–540. [Google Scholar] [CrossRef]
Variable | No (%) a |
---|---|
Age, years b | 67.5 (IQR, 57.3–75.8) |
Male | 33 (75) |
Charlson Index b | 3.0 (IQR, 0.0–4.0) |
Comorbidities | |
Diabetes mellitus | 13 (29.5) |
Oncologic diseases | 8 (18.2) |
Renal insufficiency | 3 (6.8) |
Immunosuppressive treatment | 2 (4.5) |
Others | 14 (31.8) |
Time to diagnosis, days b | 78.0 (IQR, 10.0–431.0) |
Previous prosthesis | 5 (11.4) |
Previous surgery | 5 (11.4) |
Previous infections | 5 (11.4) |
Prosthesis infection | |
Right shoulder | 24 (54.5) |
Left shoulder | 20 (45.5) |
Clinical characteristics | |
Fever | 8 (18.2) |
Joint pain | 33 (75) |
Swelling | 23 (52.3) |
Fistula | 7 (15.9) |
Purulent wound drainage | 12 (27.3) |
Laboratory parameters b | |
WBC count, cells/mm3 | 8245.0 (IRQ, 6427.5–10,367.5) |
CRP, mg/dL | 14.0 (IQR, 6.0–32.3) |
ESR, mm/h | 46.0 (IQR, 22.0–71.0) |
Type of shoulder PJI | |
• Tsukayama classification | |
Early postoperative infection | 11 (25.0) |
Late chronic infection | 27 (61.4) |
Positive intraoperative infection | 6 (13.6) |
• Zimmerli classification | |
Early infection | 23 (52.3) |
Delayed or low-grade infection | 14 (31.8) |
Late infection | 7 (15.9) |
Variable | Patients No. (%) a |
---|---|
Samples taken for culture | |
Joint aspirate fluid | 17 (38.6) |
Intraoperative sample | 42 (95.5) |
Joint fluid + intraoperative samples | 15 (34.1) |
Microorganisms isolated | |
Only P. acnes | 35 (79.5) |
Co-infection with S. epidermidis | 9 (20.5) |
Microbial susceptibility b | |
Penicillin | 39 (100) |
Vancomycin | 27 (100) |
Clindamycin | 38 (97.4) |
Tetracycline | 13 (100) |
Rifampin | 23 (100) |
Treatment | Type of Infection No. (%) a | Total (n = 44) | p | ||
---|---|---|---|---|---|
Type 4 b (n = 6) | Type 2 b (n = 27) | Type 1 b (n = 11) | |||
Antibiotic | |||||
Amoxicillin | 3 (50.0) | 13 (48.1) | 3 (27.3) | 19 (43.2) | 0.558 |
Clindamycin | 3 (50.0) | 8 (29.6) | 3 (27.3) | 14 (31.8) | 0.650 |
Rifampin | 2 (33.3) | 11 (40.7) | 6 (54.5) | 19 (43.2) | 0.677 |
Surgical | |||||
Debridement and retention | 0 | 6 (22.2) | 10 (90.9) | 16 (36.4) | 0.000 |
2-stage procedure | 1 (16.7) | 15 (55.6) | 1 (9.1) | 17 (38.6) | 0.013 |
1-stage procedure | 4 (66.7) | 4 (14.8) | 0 (0) | 8 (18.2) | 0.006 |
Arthrodesis | 0 | 1 (3.7) | 0 (0) | 1 (2.3) | 1 |
Resection arthroplasty | 1 (16.7) | 1 (3.7) | 0 (0) | 2 (4.5) | 0.315 |
Outcome | |||
---|---|---|---|
Variable | Cured (N = 34) | Recurrence (N = 5) | p |
Age, years (Median) | 68 (IQR, 57.8–76.3) | 69 (IQ, 42.5–73.5) | 0.378 |
Gender, No. (%) | |||
Male | 24 (70.6) | 5 (100) | 0.302 |
Female | 10 (29.4) | 0 (0) | |
Charlson Index (Median) | 2.95 (IQR, 0–4.03) | 2.0 (IQR, 0–4.50) | 0.729 |
Comorbidities, No. (%) | |||
Diabetes | 8 (23.5) | 3 (60) | 0.125 |
Renal insufficiency | 2 (5.9) | 1 (20) | 0.345 |
Oncologic disease | 7 (20.6) | 0.563 | |
Immunosuppressive therapy | 2 (5.9) | 1 | |
Previous prosthesis, No. (%) | 3 (8.8) | 2 (40) | 0.114 |
Previous surgery, No. (%) | 2 (5.9) | 2 (40) | 0.072 |
Previous infections, No. (%) | 2 (5.9) | 2 (40) | 0.072 |
Prosthesis infection, No. (%) | |||
Right shoulder | 18 (53) | 3 (60) | 1 |
Left shoulder | 16 (47) | 2 (40) | |
Time to diagnosis, days (Median) | 67 (IQR, 9–199) | 70 (IQR, 7–1537) | 0.823 |
Type of infection No. (%) | |||
• Tsukayama classification | 1 | ||
Early postoperative infection | 10 (29.4) | 1 (20.0) | |
Late chronic infection | 20 (58.8) | 3 (60.0) | |
Positive intraoperative cultures | 4 (11.8) | 1 (20.0) | |
• Zimmerli classification | 0.823 | ||
Early infection | 19 (55.9) | 3 (60) | |
Delayed or low-grade infection | 11 (32.4) | 1 (20) | |
Late infection | 4 (11.8) | 1 (20) | |
Surgical treatment, No. (%) | |||
Prosthesis retention | 13 (38.2) | 2 (40) | 1 |
1-stage procedure | 5 (14.7) | 1 (20) | 1 |
2-stage procedure | 13 (38.2) | 2 (40) | 1 |
Arthrodesis | 1 (2.9) | 0 | 1 |
Resection arthroplasty | 2 (5.9) | 0 | 1 |
Antimicrobial treatment, No. (%) | |||
Amoxicillin | 14 (41.2) | 1 (20) | 0.631 |
Clindamycin | 3 (8.8) | 2 (40) | 0.114 |
Other | 2 (5.9) | 0 | 1 |
Amoxicillin plus rifampin | 3 (8.8) | 1 (20) | 0.436 |
Clindamycin plus rifampin | 5 (14.7) | 1 (20) | 1 |
Other plus rifampin | 7 (20.6) | 0 | 0.563 |
Patient | Age, Years a | Sex | Comorbid Factors | Clinical Signs and Symptoms | Delay in Diagnosis, Days | Type of Infection | Treatment | |||
---|---|---|---|---|---|---|---|---|---|---|
Tsukayama b | Zimmerli | Type of Surgery | Antibiotic Regimen | Duration, Days | ||||||
1 | 69 | Male | Fever | 407 | Type 2 | Delayed infection | 1-stage procedure | Amoxicillin | 57 | |
2 | 74 | Male | DM, CKD | Joint pain, joint swelling | 70 | Type 2 | Early infection | DAIR | Amoxicillin plus Rifampin | 138 |
3 | 52 | Male | DM | Joint pain, joint swelling, fistula | 2667 | Type 2 | Late infection | 2-stage procedure | Clindamycin plus Rifampin | 112 |
4 | 73 | Male | DM | 0 | Type 4 | Early infection | 2-stage procedure | Clindamycin | 60 | |
5 | 33 | Male | Joint pain, joint swelling, fistula, purulent wound drainage | 14 | Type 1 | Early infection | DAIR | Clindamycin | 175 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Vilchez, H.H.; Escudero-Sanchez, R.; Fernandez-Sampedro, M.; Murillo, O.; Auñón, Á.; Rodríguez-Pardo, D.; Jover-Sáenz, A.; del Toro, M.D.; Rico, A.; Falgueras, L.; et al. Prosthetic Shoulder Joint Infection by Cutibacterium acnes: Does Rifampin Improve Prognosis? A Retrospective, Multicenter, Observational Study. Antibiotics 2021, 10, 475. https://doi.org/10.3390/antibiotics10050475
Vilchez HH, Escudero-Sanchez R, Fernandez-Sampedro M, Murillo O, Auñón Á, Rodríguez-Pardo D, Jover-Sáenz A, del Toro MD, Rico A, Falgueras L, et al. Prosthetic Shoulder Joint Infection by Cutibacterium acnes: Does Rifampin Improve Prognosis? A Retrospective, Multicenter, Observational Study. Antibiotics. 2021; 10(5):475. https://doi.org/10.3390/antibiotics10050475
Chicago/Turabian StyleVilchez, Helem H., Rosa Escudero-Sanchez, Marta Fernandez-Sampedro, Oscar Murillo, Álvaro Auñón, Dolors Rodríguez-Pardo, Alfredo Jover-Sáenz, Mª Dolores del Toro, Alicia Rico, Luis Falgueras, and et al. 2021. "Prosthetic Shoulder Joint Infection by Cutibacterium acnes: Does Rifampin Improve Prognosis? A Retrospective, Multicenter, Observational Study" Antibiotics 10, no. 5: 475. https://doi.org/10.3390/antibiotics10050475
APA StyleVilchez, H. H., Escudero-Sanchez, R., Fernandez-Sampedro, M., Murillo, O., Auñón, Á., Rodríguez-Pardo, D., Jover-Sáenz, A., del Toro, M. D., Rico, A., Falgueras, L., Praena-Segovia, J., Guío, L., Iribarren, J. A., Lora-Tamayo, J., Benito, N., Morata, L., Ramirez, A., Riera, M., Study Group on Osteoarticular Infections (GEIO), & the Spanish Network for Research in Infectious Pathology (REIPI). (2021). Prosthetic Shoulder Joint Infection by Cutibacterium acnes: Does Rifampin Improve Prognosis? A Retrospective, Multicenter, Observational Study. Antibiotics, 10(5), 475. https://doi.org/10.3390/antibiotics10050475