journal article·2026-07-14Open access

Biomaterial-Driven Modulation of Macrophage Polarization in an Experimental Environment of Implant-Associated Infection Mediated by Staphylococcus aureus: A Systematic Review of Preclinical Studies

Giorgia Codispoti, Maria Sartori, Michael Salvatore, Andrea Liberatore, Liliana Gabrielli, Tiziana Lazzarotto, Gianluca Giavaresi

Abstract

Implant-associated infections (IAIs) caused by Staphylococcus aureus are a major cause of orthopedic implant failure, driven by biofilm formation and chronic inflammation. Macrophages regulate bacterial clearance and tissue repair through polarization into pro-inflammatory (M1) and anti-inflammatory (M2) phenotypes. This systematic review evaluated preclinical in vivo studies according to PICO criteria (Population: IAI animal models; Intervention: functionalized biomaterials; Comparator: non-functionalized controls; Outcome: bacterial burden reduction associated with macrophage reprogramming). A PRISMA-guided search of PubMed, Scopus, Web of Science, and Embase (January 2015–December 2025) identified 23 eligible studies, assessed using SYRCLE’s risk-of-bias tool. Due to heterogeneity, a narrative synthesis was performed without meta-analysis. Effect measures included bacterial CFU reduction, macrophage polarization markers, cytokine expression, and histological outcomes. In 87.5% of studies, macrophage modulation was associated with reduced bacterial load, biofilm disruption, and improved peri-implant tissue repair and bone integration. These findings support immunomodulatory biomaterials as promising strategies to manage IAIs through combined antibacterial and immune-regulatory mechanisms. However, further validation in larger animal models is required, particularly for nanomaterials. The protocol of this systematic review was registered on the Open Science Framework.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Orthopedic Infections and Treatments · Bone Tissue Engineering Materials · Bone fractures and treatments

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Surgical Sciences and Technologies, IRCCS Istituto Ortopedico Rizzoli, Via di Barbiano, 1/10, 40136 Bologna, Italy

Microbiology Unit, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Via Massarenti 9, 40138 Bologna, Italy

Department of Medical and Surgical Sciences, Alma Mater Studiorum, University of Bologna, Via Massarenti 9, 40138 Bologna, Italy

References (100+)

Show source-provided references
1. Current developments in orthopaedic implant technology10.1186/s13018-025-06279-w ↗
2. Antibacterial hydrogel coating in joint mega-prosthesis: Results of a comparative series10.1007/s00590-021-02884-7 ↗
3. Psychological and social aspects in orthopaedics and trauma surgery, challenges and solutions in trauma: A didactic overview10.1530/EOR-2025-0054 ↗
4. Ayoade, F., Li, D., Mabrouk, A., and Todd, J.R. (2026). Periprosthetic Joint Infection. StatPearls, StatPearls Publishing.
5. Verhaar, J.a.N., Kjærsgaard-Andersen, P., Limb, D., Günther, K.-P., and Karachalios, T. (2021). B|Surgical Treatment. The EFORT White Book: “Orthopaedics and Traumatology in Europe”, Dennis Barber Ltd.
6. Periprosthetic Joint Infection: A Multifaceted Burden Undermining Arthroplasty Success10.52965/001c.138205 ↗
7. Preventive strategies to reduce the rate of periprosthetic infections in total joint arthroplasty; a comprehensive review10.1007/s00402-024-05301-w ↗
8. Grupkovic, J., Ceculovic, M., Dabetic, U., Aleksandric, D., Bogosavljevic, N., Lazovic, R., and Zagorac, S. (2025). Infection in Joint Arthroplasty: Diagnosis, Prevention, and Treatment Strategies-A Comprehensive Narrative Review. Life, 15.10.3390/life15121853 ↗
9. Moreira, P.A.M., Gontijo, T.d.C., Colen, G.C., Morganti, A.C., Ulloa Gómez, F.I., Mourão, P.A., Mota, G.A.R., Couto, B.R.G.M., Rocha, P.A.d.V., and Machado, L.G. (2025). Comparison of Cost Savings of Methods of Prevention of Orthopedic Implant-Associated Infection in Arthroplasty and Closed Fracture Surgery Patients. Antibiotics, 14.10.3390/antibiotics14090900 ↗
10. New Developments in Diagnosis and Treatment of Infection in Orthopedic Implants10.1086/321863 ↗
11. Implant infections: Adhesion, biofilm formation and immune evasion10.1038/s41579-018-0019-y ↗
12. Pietrocola, G., Campoccia, D., Motta, C., Montanaro, L., Arciola, C.R., and Speziale, P. (2022). Colonization and Infection of Indwelling Medical Devices by Staphylococcus aureus with an Emphasis on Orthopedic Implants. Int. J. Mol. Sci., 23.10.3390/ijms23115958 ↗
13. Lister, J.L., and Horswill, A.R. (2014). Staphylococcus aureus biofilms: Recent developments in biofilm dispersal. Front. Cell. Infect. Microbiol., 4.10.3389/fcimb.2014.00178 ↗
14. Pidwill, G.R., Gibson, J.F., Cole, J., Renshaw, S.A., and Foster, S.J. (2020). The Role of Macrophages in Staphylococcus aureus Infection. Front. Immunol., 11.10.3389/fimmu.2020.620339 ↗
15. Immune Evasion by Staphylococcus aureus
16. Maimaiti, Z., Li, Z., Xu, C., Fu, J., Hao, L.-B., Chen, J.-Y., and Chai, W. (2023). Host Immune Regulation in Implant-Associated Infection (IAI): What Does the Current Evidence Provide Us to Prevent or Treat IAI?. Bioengineering, 10.10.3390/bioengineering10030356 ↗
17. Functional plasticity of macrophages: Reversible adaptation to changing microenvironments10.1189/jlb.0504272 ↗
18. Arango Duque, G., and Descoteaux, A. (2014). Macrophage cytokines: Involvement in immunity and infectious diseases. Front. Immunol., 5.10.3389/fimmu.2014.00491 ↗
19. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo10.4049/jimmunol.1002794 ↗
20. Yamada, K.J., Heim, C.E., Xi, X., Attri, K.S., Wang, D., Zhang, W., Singh, P.K., Bronich, T.K., and Kielian, T. (2020). Monocyte metabolic reprogramming promotes pro-inflammatory activity and Staphylococcus aureus biofilm clearance. PLoS Pathog., 16.10.1371/journal.ppat.1008354 ↗
21. Wang, S., Liu, G., Li, Y., and Pan, Y. (2022). Metabolic Reprogramming Induces Macrophage Polarization in the Tumor Microenvironment. Front. Immunol., 13.10.3389/fimmu.2022.840029 ↗
22. The alterations of molecular repertoire of the RANKL-induced osteoclastogenesis in the M1 macrophage-derived inflammatory milieu10.1038/s41598-025-99772-5 ↗
23. Cong, Y., Wang, Y., Yuan, T., Zhang, Z., Ge, J., Meng, Q., Li, Z., and Sun, S. (2023). Macrophages in aseptic loosening: Characteristics, functions, and mechanisms. Front. Immunol., 14.10.3389/fimmu.2023.1122057 ↗
24. Intracellular survival of Staphylococcus aureus in macrophages during osteomyelitis10.1080/21505594.2025.2553789 ↗
25. Establishment of a reliable in-vivo model of implant-associated infection to investigate innovative treatment options10.1038/s41598-022-07673-8 ↗
26. Eradication of Staphylococcus epidermidis within Biofilms: Comparison of Systemic versus Supratherapeutic Concentrations of Antibiotics10.1128/aac.00108-23 ↗
27. Surface coating of orthopedic implant to enhance the osseointegration and reduction of bacterial colonization: A review10.1186/s40824-022-00269-3 ↗
28. Bioactive coating provides antimicrobial protection through immunomodulation and phage therapeutics10.1016/j.mtbio.2024.101022 ↗
29. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews10.1136/bmj.n71 ↗
30. Rayyan-a web and mobile app for systematic reviews10.1186/s13643-016-0384-4 ↗
31. Wang, L., Wang, Q., Wang, F., Xiong, S., Yang, X., Zhao, J., Lu, X., Zhang, Y., Chen, P., and Qian, S. (2025). Multifunctional PEEK implants via mussel adhesion-mediated assembly for osteoimmune regulation and antibacterial properties. Front. Bioeng. Biotechnol., 13.10.3389/fbioe.2025.1624106 ↗
32. Glucose-gated nanocoating endowing polyetheretherketone implants for enzymatic gas therapy to boost infectious diabetic osseointegration10.1016/j.nantod.2024.102541 ↗
33. pH-Responsive silk protein/ZIF-8@bacitracin composite coating on strontium-doped nanorod surface for combating implant-associated infections10.1016/j.ijbiomac.2025.144661 ↗
34. Mg-Co double hydroxide/lactoferrin composite coating on Ti-based orthopedic implants: A pioneering strategy for augmenting bone defect restoration10.1016/j.ijbiomac.2025.142489 ↗
35. Controlled-release of cinnamaldehyde from MXene/ZIF8/gelatin composite coatings: An integrated strategy to combat implant-associated infection10.1016/j.colsurfb.2025.114615 ↗
36. “Photo-Thermo-Electric” Dental Implant for Anti-Infection and Enhanced Osteoimmunomodulation10.1021/acsnano.4c05859 ↗
37. Ultrasound-driven radical chain reaction and immunoregulation of piezoelectric-based hybrid coating for treating implant infection10.1016/j.biomaterials.2024.122532 ↗
38. Surficial nano-deposition locoregionally yielding bactericidal super CAR-macrophages expedites periprosthetic osseointegration10.1126/sciadv.adg3365 ↗
39. Calcium Peroxide Nanoparticles-Embedded Coatings on Anti-Inflammatory TiO2 Nanotubes for Bacteria Elimination and Inflammatory Environment Amelioration10.1002/smll.202102907 ↗
40. Silver-quercetin-loaded honeycomb-like Ti-based interface combats infection-triggered excessive inflammation via specific bactericidal and macrophage reprogramming
41. Programmed surface platform orchestrates anti-bacterial ability and time-sequential bone healing for implant-associated infection10.1016/j.biomaterials.2024.122772 ↗
42. Functional Titanium Substrates Synergetic Photothermal Therapy for Enhanced Antibacterial and Osteogenic Performance via Immunity Regulation10.1002/adhm.202300494 ↗
43. Piezoelectric Nanostructured Surface for Ultrasound-Driven Immunoregulation to Rescue Titanium Implant Infection10.1002/adfm.202214522 ↗
44. Novel Titanium Implant: A 3D Multifunction Architecture with Charge-Trapping and Piezoelectric Self-Stimulation10.1002/adhm.202202620 ↗
45. Using a degradable three-layer sandwich-type coating to prevent titanium implant infection with the combined efficient bactericidal ability and fast immune remodeling property10.1016/j.actbio.2022.10.033 ↗
46. Elimination of methicillin-resistant Staphylococcus aureus biofilms on titanium implants via photothermally-triggered nitric oxide and immunotherapy for enhanced osseointegration
47. Amplified copper ion interference and immunomodulation using self-thermophoretic nanomotors to treat refractory implant-associated biofilm infections10.1038/s41467-025-64064-z ↗
48. Targeted Light-Induced Immunomodulatory Strategy for Implant-Associated Infections via Reversing Biofilm-Mediated Immunosuppression10.1021/acsnano.3c10172 ↗
49. A novel antibacterial immune activator: Bi-MOF acts as H2S scavenger to suppress HIF-1α S-sulfhydration and alleviate implant-associated infection10.1016/j.nantod.2024.102334 ↗
50. Drug delivery nanoparticles for preventing implant bacterial infections based on the bacteria and immunity mechanisms10.1039/D3BM01584J ↗
51. Enzymatic bionanocatalysts for combating peri-implant biofilm infections by specific heat-amplified chemodynamic therapy and innate immunomodulation10.1016/j.drup.2022.100917 ↗
52. Inorganic nanosheets facilitate humoral immunity against medical implant infections by modulating immune co-stimulatory pathways10.1038/s41467-022-32405-x ↗
53. Hooijmans, C.R., Rovers, M.M., de Vries, R.B., Leenaars, M., Ritskes-Hoitinga, M., and Langendam, M.W. (2014). SYRCLE’s risk of bias tool for animal studies. BMC Med. Res. Methodol., 14.10.1186/1471-2288-14-43 ↗
54. Targeting macrophage activation for the prevention and treatment of Staphylococcus aureus biofilm infections10.4049/jimmunol.1202348 ↗
55. Macrophages in tissue repair, regeneration, and fibrosis10.1016/j.immuni.2016.02.015 ↗
56. Brancewicz, J., Wójcik, N., Sarnowska, Z., Robak, J., and Król, M. (2025). The Multifaceted Role of Macrophages in Biology and Diseases. Int. J. Mol. Sci., 26.10.3390/ijms26052107 ↗
57. Regulation of Macrophage Polarization Through Periodic Photo-Thermal Treatment to Facilitate Osteogenesis10.1002/smll.202202691 ↗
58. Near-Infrared Switch-Driven Macrophage Dynamically Reprogramming for Anti-Infection and Tissue Healing on Polyetheretherketone Implants10.1002/advs.202512592 ↗
59. A biomimetic upconversion nanoreactors for near-infrared driven H2 release to inhibit tauopathy in Alzheimer’s disease therapy
60. Remote eradication of biofilm on titanium implant via near-infrared light triggered photothermal/photodynamic therapy strategy10.1016/j.biomaterials.2019.119479 ↗
61. Anti-Inflammatory Effects Induced by Near-Infrared Light Irradiation through M2 Macrophage Polarization10.1016/j.jid.2020.11.035 ↗
62. Photobiomodulation activates undifferentiated macrophages and promotes M1/M2 macrophage polarization via PI3K/AKT/mTOR signaling pathway10.1007/s10103-023-03753-x ↗
63. Macrophages Modulated by Red/NIR Light: Phagocytosis, Cytokines, Mitochondrial Activity, Ca2+ Influx, Membrane Depolarization and Viability10.1111/php.13526 ↗
64. Galván-Peña, S., and O’Neill, L.A.J. (2014). Metabolic Reprograming in Macrophage Polarization. Front. Immunol., 5.10.3389/fimmu.2014.00420 ↗
65. Glycolysis—A key player in the inflammatory response10.1111/febs.15327 ↗
66. Viola, A., Munari, F., Sánchez-Rodríguez, R., Scolaro, T., and Castegna, A. (2019). The Metabolic Signature of Macrophage Responses. Front. Immunol., 10.10.3389/fimmu.2019.01462 ↗
67. Akt Signaling Pathway in Macrophage Activation and M1/M2 Polarization10.4049/jimmunol.1601515 ↗
68. Akt1-mediated regulation of macrophage polarization in a murine model of Staphylococcus aureus pulmonary infection10.1093/infdis/jit177 ↗
69. Yin, C., Cai, J., Gou, Y., Li, D., Tang, H., Wang, L., Liu, H., and Luo, B. (2022). Dynamic changes in human THP-1-derived M1-to-M2 macrophage polarization during Thelazia callipaeda MIF induction. Front. Immunol., 13.10.3389/fimmu.2022.1078880 ↗
70. Defect-Engineered Biomimetic Piezoelectric Nanocomposites With Enhanced ROS Production, Macrophage Re-polarization, and Ca2+ Channel Activation for Therapy of MRSA-Infected Wounds and Osteomyelitis10.1002/smll.202411906 ↗
71. Barium titanate piezoelectric nanoparticles induce M1 polarization in mouse macrophages via ultrasound in vitro10.1038/s41598-025-23364-6 ↗
72. Ion-incorporated titanium implants for staged regulation of antibacterial activity and immunoregulation-mediated osteogenesis10.1039/D3NR05858A ↗
73. Bioinspired Hybrid Nanostructured PEEK Implant with Enhanced Antibacterial and Anti-inflammatory Synergy10.1021/acsami.4c06322 ↗
74. Engineering immunomodulatory and osteoinductive implant surfaces via mussel adhesion-mediated ion coordination and molecular clicking10.1038/s41467-021-27816-1 ↗
75. The multifaceted roles of macrophages in bone regeneration: A story of polarization, activation and time10.1016/j.actbio.2021.04.052 ↗
76. Macrophages as Multifaceted Orchestrators of Tissue Repair: Bridging Inflammation, Regeneration, and Therapeutic Innovation10.2147/JIR.S527764 ↗
77. Emerging non-antibiotic strategies for implant-associated biofilm infections by reprogramming the dysregulated immune microenvironment10.1038/s41522-025-00907-3 ↗
78. Adoptive transfer of immunomodulatory macrophages reduces the pro-inflammatory microenvironment and increases bone formation on titanium implants10.1016/j.actbio.2024.09.011 ↗
79. Improved implant osseointegration of a nanostructured titanium surface via mediation of macrophage polarization10.1016/j.biomaterials.2014.08.025 ↗
80. Feldman, D. (2021). The Effect of Size of Materials Formed or Implanted In Vivo on the Macrophage Response and the Resultant Influence on Clinical Outcome. Materials, 14.10.3390/ma14164572 ↗
81. Size- and shape-dependent foreign body immune response to materials implanted in rodents and non-human primates10.1038/nmat4290 ↗
82. Importance of the pig as a human biomedical model10.1126/scitranslmed.abd5758 ↗
83. In vivo models of infection: Large animals—Mini review on human-scale one-stage revision in a porcine osteomyelitis model10.1016/j.injury.2024.111842 ↗
84. The pig as a model for immunology research10.1007/s00441-020-03206-9 ↗
85. Animal Models of Orthopedic Implant-Associated Infections and Revisions10.1021/acsbiomaterials.4c02331 ↗
86. Sex differences in immune responses10.1038/nri.2016.90 ↗
87. Sex differences in systemic inflammation and immune function in diet-induced obesity rodent models: A systematic review10.1111/obr.13665 ↗
88. Sex differences in resident immune cell phenotype underlie more efficient acute inflammatory responses in female mice10.1182/blood-2011-03-340281 ↗
89. Animal Models for Evaluation of Bone Implants and Devices: Comparative Bone Structure and Common Model Uses10.1177/0300985815593124 ↗
90. Guideline for Preclinical Studies of Bone Infections in Large Animals Based on a Systematic Review of 316 Non-Rodent Models10.2106/JBJS.18.01369 ↗
91. Macrophage-to-osteocyte communication: Impact in a 3D in vitro implant-associated infection model10.1016/j.actbio.2024.08.005 ↗
92. Commensal microflora coating endows implants with biofilm-repellent, immunomodulatory and osteogenic properties10.1016/j.actbio.2026.01.017 ↗
93. Li, Y., Li, X., Guo, D., Meng, L., Feng, X., Zhang, Y., and Pan, S. (2024). Immune dysregulation and macrophage polarization in peri-implantitis. Front. Bioeng. Biotechnol., 12.10.3389/fbioe.2024.1291880 ↗
94. Rahnama-Hezavah, M., Mertowska, P., Mertowski, S., Skiba, J., Krawiec, K., Łobacz, M., and Grywalska, E. (2023). How Can Imbalance in Oral Microbiota and Immune Response Lead to Dental Implant Problems?. Int. J. Mol. Sci., 24.10.3390/ijms242417620 ↗
95. Huang, M., Wang, C., Li, P., Lu, H., Li, A., and Xu, S. (2024). Role of immune dysregulation in peri-implantitis. Front. Immunol., 15.10.3389/fimmu.2024.1466417 ↗
96. Albrektsson, T., Tengvall, P., Amengual, L., Coli, P., Kotsakis, G.A., and Cochran, D. (2022). Osteoimmune regulation underlies oral implant osseointegration and its perturbation. Front. Immunol., 13.10.3389/fimmu.2022.1056914 ↗
97. Niche Specific Microbiota-Dependent and Independent Bone Loss around Dental Implants and Teeth10.1177/0022034520920577 ↗
98. Nanomaterial-based strategies to modulate macrophage polarization in osteoarthritis: A systematic review10.1016/j.bioadv.2025.214662 ↗
99. The interaction between nanoparticles and immune system: Application in the treatment of inflammatory diseases10.1186/s12951-022-01343-7 ↗
100. Current understanding of interactions between nanoparticles and the immune system10.1016/j.taap.2015.12.022 ↗