Promising applications of D-amino acids in periprosthetic joint infection

Abstract

Due to the rise in our aging population, a disproportionate demand for total joint arthroplasty (TJA) in the elderly is forecast. Periprosthetic joint infection (PJI) represents one of the most challenging complications that can occur following TJA, and as the number of primary and revision TJAs continues to rise, an increasing PJI burden is projected. Despite advances in operating room sterility, antiseptic protocols, and surgical techniques, approaches to prevent and treat PJI remain difficult, primarily due to the formation of microbial biofilms. This difficulty motivates researchers to continue searching for an effective antimicrobial strategy. The dextrorotatory-isoforms of amino acids (D-AAs) are essential components of peptidoglycan within the bacterial cell wall, providing strength and structural integrity in a diverse range of species. Among many tasks, D-AAs regulate cell morphology, spore germination, and bacterial survival, evasion, subversion, and adhesion in the host immune system. When administered exogenously, accumulating data have demonstrated that D-AAs play a pivotal role against bacterial adhesion to abiotic surfaces and subsequent biofilm formation; furthermore, D-AAs have substantial efficacy in promoting biofilm disassembly. This presents D-AAs as promising and novel targets for future therapeutic approaches. Despite their emerging antibacterial efficacy, their role in disrupting PJI biofilm formation, the disassembly of established TJA biofilm, and the host bone tissue response remains largely unexplored. This review aims to examine the role of D-AAs in the context of TJAs. Data to date suggest that D-AA bioengineering may serve as a promising future strategy in the prevention and treatment of PJI.

References

[1] Simpson, AHRW. Incidence, complications and novel treatment strategies: joint arthroplasty. In: Musculoskeletal Infection. Springer International Publishing; 2022:227–282. https://doi.org/10.1007/978-3-030-83251-3_8

[2] Williams SN, Wolford ML, Bercovitz A. Hospitalization for total knee replacement among inpatients aged 45 and over:United States, 2000–2010. NCHS Data Brief, 2015, 210: 1-8

[3] Wolford ML, Palso K, Bercovitz A. Hospitalization for total hip replacement among inpatients aged 45 and over: United States, 2000–2010. NCHS Data Brief, 2015, 210: 1-8

[4] Hooper G, Lee AJ-J, Rothwell A, Frampton C. Current trends and projections in the utilisation rates of hip and knee replacement in New Zealand from 2001 to 2026. NZ Med. J., 2014, 127: 82-93

[5] Kaufman M, Meaike J, Izaddoost S. Orthopedic prosthetic infections: diagnosis and orthopedic salvage. Semin. Plast. Surg., 2016, 30: 066-072

[6] Kurtz S, Ong K, Lau E, Mowat F, Halpern M. Projections of primary and revision hip and knee arthroplasty in the United States from 2005 to 2030. J. Bone Jt. Surg., 2007, 89: 780-785

[7] Day JS et al. Prevalence and projections of total shoulder and elbow arthroplasty in the United States to 2015. J. Shoulder Elb. Surg., 2010, 19: 1115-1120

[8] Padegimas EM et al. Future patient demand for shoulder arthroplasty by younger patients: national projections. Clin. Orthop. Relat. Res., 2015, 473: 1860-1867

[9] Kurtz SM et al. Primary and revision arthroplasty surgery caseloads in the United States from 1990 to 2004. J. Arthroplast., 2009, 24: 195-203

[10] Sloan M, Premkumar A, Sheth NP. Projected volume of primary total joint arthroplasty in the U.S., 2014 to 2030. J. Bone Jt. Surg., 2018, 100: 1455-1460

[11] Sloan, M., Sheth, N. Projected volume of primary and revision total joint arthroplasty in the United States, 2030–2060. In: Proc. Annual Meeting of the American Academy of Orthopaedic Surgeons; 2018:16.

[12] Kurtz SM et al. Future young patient demand for primary and revision joint replacement: national projections from 2010 to 2030. Clin. Orthop. Relat. Res., 2009, 467: 2606-2612

[13] Singh JA, Yu S, Chen L, Cleveland JD. Rates of total joint replacement in the united states: future projections to 2020–2040 using the national inpatient sample. J. Rheumatol., 2019, 46: 1134-1140

[14] Christensen K, Doblhammer G, Rau R, Vaupel JW. Ageing populations: the challenges ahead. Lancet, 2009, 374: 1196-1208

[15] Lee SB, Oh JH, Park JH, Choi SP, Wee JH. Differences in youngest-old, middle-old, and oldest-old patients who visit the emergency department. Clin. Exp. Emerg. Med., 2018, 5: 249-255

[16] Oeppen J, Vaupel JW. Broken limits to life expectancy. Science, 2002, 296: 1029-1031

[17] Keely Boyle K, Rachala S, Nodzo SR. Centers for disease control and prevention 2017 guidelines for prevention of surgical site infections: review and relevant recommendations. Curr. Rev. Musculoskelet. Med., 2018, 11: 357-369

[18] Springer BD, Cahue S, Etkin CD, Lewallen DG, McGrory BJ. Infection burden in total hip and knee arthroplasties: an international registry-based perspective. Arthroplast. Today, 2017, 3: 137-140

[19] Delanois RE et al. Current epidemiology of revision total knee arthroplasty in the United States. J. Arthroplast., 2017, 32: 2663-2668

[20] Krukhaug Y, Hallan G, Dybvik E, Lie SA, Furnes ON. A survivorship study of 838 total elbow replacements: a report from the Norwegian Arthroplasty Register 1994-2016. J. Shoulder Elb. Surg., 2018, 27: 260-269

[21] Moriarty TF et al. Orthopaedic device-related infection: current and future interventions for improved prevention and treatment. EFORT Open Rev., 2016, 1: 89-99

[22] Kunutsor SK, Whitehouse MR, Blom AW, Beswick AD. Patient-related risk factors for periprosthetic joint infection after total joint arthroplasty: a systematic review and meta-analysis. PLoS One, 2016, 11: e0150866

[23] Phillips JE, Crane TP, Noy M, Elliott TSJ, Grimer RJ. The incidence of deep prosthetic infections in a specialist orthopaedic hospital. J. Bone Jt. Surg. Br., 2006, 88-B: 943-948

[24] Krenek L, Farng E, Zingmond D, SooHoo NF. Complication and revision rates following total elbow arthroplasty. J. Hand Surg. Am., 2011, 36: 68-73

[25] VanEpps JS, Younger JG. Implantable device-related infection. Shock, 2016, 46: 597-608

[26] Lentino JR. Prosthetic joint infections: bane of orthopedists, challenge for infectious disease specialists. Clin. Infect. Dis., 2003, 36: 1157-1161

[27] Tribble DR et al. Infection-associated clinical outcomes in hospitalized medical evacuees after traumatic injury: trauma infectious disease outcome study. J. Trauma Inj. Infect. Crit. Care, 2011, 71: S33-S42

[28] Ryan DJ, Minhas SV, Konda S, Catalano LW. Surgical site infection after open upper extremity fracture and the effect of urgent operative intervention. J. Orthop. Trauma, 2020, 34: 258-262

[29] Jaekel, D. J., Ong, K. L., Lau, E. C., Watson, H. N., Kurtz, S. M. Epidemiology of total hip and knee arthroplasty infection. In: Proc. Periprosthetic Joint Infection of the Hip and Knee. Springer New York; 2014:1–14. https://doi.org/10.1007/978-1-4614-7928-4_1

[30] Coraça-Huber DC et al. Identification and morphological characterization of biofilms formed by strains causing infection in orthopedic implants. Pathogens, 2020, 9: 649

[31] Varacallo, M., Luo, T. D., Johanson, N. A. Total hip arthroplasty techniques; 2022.

[32] Crémet L et al. Pathogenic potential of Escherichia coli clinical strains from orthopedic implant infections towards human osteoblastic cells. Pathog. Dis., 2015, 73: ftv065

[33] Chen M-F et al. Rapid analysis of bacterial composition in prosthetic joint infection by 16S rRNA metagenomic sequencing. Bone Jt. Res., 2019, 8: 367-377

[34] Tande AJ, Patel R. Prosthetic joint infection. Clin. Microbiol. Rev., 2014, 27: 302-345

[35] Ascione T et al. General assembly, diagnosis, pathogen isolation—culture matters: proceedings of international consensus on orthopedic infections. J. Arthroplast., 2019, 34: S197-S206

[36] Rosteius T et al. Evaluating the microbial pattern of periprosthetic joint infections of the hip and knee. J. Med. Microbiol., 2018, 67: 1608-1613

[37] Parvizi J et al. Resistant organisms in infected total knee arthroplasty: occurrence, prevention, and treatment regimens. Instr. Course Lect., 2009, 58: 271-278

[38] Murray CJ et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet, 2022, 399: 629-655

[39] Tsukayama DT, Goldberg VM, Kyle R. Diagnosis and management of infection after total knee arthroplasty. J. Bone Jt Surg.-Am., 2003, 85: 75-80

[40] McPherson EJ et al. Outcome of infected total knee utilizing a staging system for prosthetic joint infection. Am. J. Orthop., 1999, 28: 161-165

[41] Izakovicova P, Borens O, Trampuz A. Periprosthetic joint infection: current concepts and outlook. EFORT Open Rev., 2019, 4: 482-494

[42] Zimmerli W. Clinical presentation and treatment of orthopaedic implant-associated infection. J. Intern Med, 2014, 276: 111-119

[43] Murdoch DR et al. Infection of orthopedic prostheses after Staphylococcus aureus bacteremia. Clin. Infect. Dis., 2001, 32: 647-649

[44] Pulido L, Ghanem E, Joshi A, Purtill JJ, Parvizi J. Periprosthetic joint infection: the incidence, timing, and predisposing factors. Clin. Orthop. Relat. Res., 2008, 466: 1710-1715

[45] Egol KA, Gruson K, Spitzer AB, Walsh M, Tejwani NC. Do Successful surgical results after operative treatment of long-bone nonunions correlate with outcomes. Clin. Orthop. Relat. Res, 2009, 467: 2979-2985

[46] Badia JM et al. Impact of surgical site infection on healthcare costs and patient outcomes: a systematic review in six European countries. J. Hosp. Infect., 2017, 96: 1-15

[47] Chang J-D, Kim I-S, Lee S-S, Yoo J-H. Acute delayed or late infection of revision total hip arthroplasty treated with debridement/antibiotic-loaded cement beads and retention of the prosthesis. Hip Pelvis, 2017, 29: 35

[48] Bozic KJ. The impact of infection after total hip arthroplasty on hospital and surgeon resource utilization. J. Bone Jt Surg., 2005, 87: 1746

[49] Kapadia BH et al. The economic impact of periprosthetic infections following total knee arthroplasty at a specialized tertiary-care center. J. Arthroplast., 2014, 29: 929-932

[50] Garrido-Gómez J et al. Descriptive analysis of the economic costs of periprosthetic joint infection of the knee for the public health system of Andalusia. J. Arthroplast., 2013, 28: 1057-1060

[51] Kurtz SM, Lau E, Watson H, Schmier JK, Parvizi J. Economic burden of periprosthetic joint infection in the United States. J. Arthroplast., 2012, 27: 61-65.e1

[52] Padegimas EM et al. Periprosthetic shoulder infection in the United States: incidence and economic burden. J. Shoulder Elb. Surg., 2015, 24: 741-746

[53] Eckers F et al. Risk factor analysis for above-knee amputation in patients with periprosthetic joint infection of the knee: a case-control study. BMC Musculoskelet. Disord., 2021, 22

[54] Robertsson O, Ranstam J, Sundberg M, W-Dahl A, Lidgren L. The Swedish knee arthroplasty register. Bone Jt. Res., 2014, 3: 217-222

[55] Fisman DN, Reilly DT, Karchmer AW, Goldie SJ. Clinical effectiveness and cost-effectiveness of 2 management strategies for infected total hip arthroplasty in the elderly. Clin. Infect. Dis., 2001, 32: 419-430

[56] Natsuhara KM, Shelton TJ, Meehan JP, Lum ZC. Mortality during total hip periprosthetic joint infection. J. Arthroplast., 2019, 34: S337-S342

[57] Stanton T. PJI & cancer: more similar than different? Am. Assoc. Orthop. Surg. Published online August 2017.

[58] Teterycz D et al. Outcome of orthopedic implant infections due to different staphylococci. Int. J. Infect. Dis., 2010, 14: e913-e918

[59] Shah NB et al. Pseudomonas prosthetic joint infections: a review of 102 episodes. J. Bone Jt Infect., 2016, 1: 25-30

[60] Bian T, Shao H, Zhou Y, Huang Y, Song Y. Tests for predicting reimplantation success of two-stage revision for periprosthetic joint infection: a systematic review and meta-analysis. Orthop. Traumatol. Surg. Res., 2018, 104: 1115-1123

[61] Zardi EM, Franceschi F. Prosthetic joint infection. A relevant public health issue. J. Infect. Public Health, 2020, 13: 1888-1891

[62] Jeyanathan A et al. Lactobacillus cell‐free supernatant as a novel bioagent and biosurfactant against Pseudomonas aeruginosa in the prevention and treatment of orthopedic implant infection. J. Biomed. Mater. Res. Part B Appl. Biomater., 2021, 109: 1634-1643

[63] Pugazhendhi, A. S., Wei, F., Hughes, M., Coathup, M. Bacterial adhesion, virulence, and biofilm formation. In: Musculoskeletal Infection. Springer International Publishing; 19–64. https://doi.org/10.1007/978-3-030-83251-3_2 (2022).

[64] Yin W, Wang Y, Liu L, He J. Biofilms: the microbial “protective clothing” in extreme environments. Int. J. Mol. Sci., 2019, 20: 3423

[65] Ribeiro M, Monteiro FJ, Ferraz MP. Infection of orthopedic implants with emphasis on bacterial adhesion process and techniques used in studying bacterial-material interactions. Biomatter, 2012, 2: 176-194

[66] Song Z et al. Prosthesis infections after orthopedic joint replacement: the possible role of bacterial biofilms. Orthop. Rev., 2013, 5: 14

[67] Luepke KH et al. Past, present, and future of antibacterial economics: increasing bacterial resistance, limited antibiotic pipeline, and societal implications. Pharmacother. J. Hum. Pharm. Drug Ther., 2017, 37: 71-84

[68] Miyamoto T, Homma H. D-Amino acid metabolism in bacteria. J. Biochem, 2021, 170: 5-13

[69] Mathur H et al. Bacteriocin-antimicrobial synergy: a medical and food perspective. Front. Microbiol, 2017, 8: 1205

[70] Meade Slattery, Garvey. Bacteriocins, potent antimicrobial peptides and the fight against multi drug resistant species: resistance is futile? Antibiotics, 2020, 9: 32

[71] Balzarini J et al. Pradimicin S, a highly soluble nonpeptidic small-size carbohydrate-binding antibiotic, Is an anti-HIV drug lead for both microbicidal and systemic use. Antimicrob. Agents Chemother., 2010, 54: 1425-1435

[72] Thakur P et al. Rhamnolipid the Glycolipid Biosurfactant: emerging trends and promising strategies in the field of biotechnology and biomedicine. Micro. Cell Fact., 2021, 20: 1

[73] Amaning Danquah C, Minkah PAB, Osei Duah Junior I, Amankwah KB, Somuah SO. Antimicrobial compounds from microorganisms. Antibiotics, 2022, 11: 285

[74] Santovito E et al. Antimicrobial activity of yeast cell wall products against Clostridium perfringens. Foodborne Pathog. Dis., 2019, 16: 638-647

[75] Beutler B. Pathogens, commensals, and immunity: from the perspective of the urinary bladder. Pathogens, 2016, 5: 5

[76] LeBel G, Piché F, Frenette M, Gottschalk M, Grenier D. Antimicrobial activity of nisin against the swine pathogen Streptococcus suis and its synergistic interaction with antibiotics. Peptides, 2013, 50: 19-23

[77] Carroll J et al. Comparison of the activities of the lantibiotics nisin and lacticin 3147 against clinically significant mycobacteria. Int. J. Antimicrob. Agents, 2010, 36: 132-136

[78] Deliorman, Orhan D. Bacteriocins produced by probiotic microorganisms. In: Advances in Probiotics. Elsevier; 2021:277–291. https://doi.org/10.1016/B978-0-12-822909-5.00018-6

[79] Tymoszewska A, Diep DB, Wirtek P, Aleksandrzak-Piekarczyk T. The non-lantibiotic bacteriocin garvicin Q targets Man-PTS in a broad spectrum of sensitive bacterial genera. Sci. Rep., 2017, 7

[80] Zalán Z, Hudáček J, Štětina J, Chumchalová J, Halász A. Production of organic acids by Lactobacillus strains in three different media. Eur. Food Res. Technol., 2010, 230: 395-404

[81] Punia Bangar S, Suri S, Trif M, Ozogul F. Organic acids production from lactic acid bacteria: a preservation approach. Food Biosci., 2022, 46: 101615

[82] Hernández-González JC, Martínez-Tapia A, Lazcano-Hernández G, García-Pérez BE, Castrejón-Jiménez NS. Bacteriocins from lactic acid bacteria. a powerful alternative as antimicrobials, probiotics, and immunomodulators in veterinary medicine. Animals, 2021, 11: 979

[83] Paiva AD, Breukink E, Mantovani HC. Role of lipid II and membrane thickness in the mechanism of action of the lantibiotic bovicin HC5. Antimicrob. Agents Chemother., 2011, 55: 5284-5293

[84] Parada JL, Caron CR, Medeiros ABP, Soccol CR. Bacteriocins from lactic acid bacteria: purification, properties and use as biopreservatives. Braz. Arch. Biol. Technol., 2007, 50: 512-542

[85] Perez, R. H., Zendo, T., Sonomoto, K. Circular and leaderless bacteriocins: biosynthesis, mode of action, applications, and prospects. Front. Microbiol. 9, 2085 (2018).

[86] Zhang L et al. Evaluation of Lactobacillus rhamnosus GG using an Escherichia coli K88 model of piglet diarrhoea: effects on diarrhoea incidence, faecal microflora and immune responses. Vet. Microbiol., 2010, 141: 142-148

[87] Alexandre Y, Le Berre R, Barbier G, Le Blay G. Screening of Lactobacillus spp. for the prevention of Pseudomonas aeruginosa pulmonary infections. BMC Microbiol., 2014, 14: 107

[88] Zhou, B., Zhang D. Antibacterial effects of bacteriocins isolated from Lactobacillus rhamnosus (ATCC 53103) in a rabbit model of knee implant infection. Exp. Ther. Med. 15, 2985–2989 (2018).

[89] Ouwehand, A. C., Salminen, S., Isolauri, E. Probiotics: an overview of beneficial effects. In: Lactic Acid Bacteria: Genetics, Metabolism and Applications. Springer Netherlands; 2002:279–289. https://doi.org/10.1007/978-94-017-2029-8_18

[90] Sikorska H, Smoragiewicz W. Role of probiotics in the prevention and treatment of meticillin-resistant Staphylococcus aureus infections. Int. J. Antimicrob. Agents, 2013, 42: 475-481

[91] da Cunha NB et al. The next generation of antimicrobial peptides (AMPs) as molecular therapeutic tools for the treatment of diseases with social and economic impacts. Drug Discov. Today, 2017, 22: 234-248

[92] Wang J et al. Antimicrobial peptides: promising alternatives in the post feeding antibiotic era. Med. Res. Rev., 2019, 39: 831-859

[93] Lakshmaiah Narayana J, Chen J-Y. Antimicrobial peptides: possible anti-infective agents. Peptides, 2015, 72: 88-94

[94] Tortorella E et al. Antibiotics from deep-sea microorganisms: current discoveries and perspectives. Mar. Drugs, 2018, 16: 355

[95] Walsh TJ, Giri N. Pradimicins: a novel class of broad-spectrum antifungal compounds. Eur. J. Clin. Microbiol. Infect. Dis., 1997, 16: 93-97

[96] Bais HP, Fall R, Vivanco JM. Biocontrol of Bacillus subtilis against Infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol., 2004, 134: 307-319

[97] Park JS, Ryu GR, Kang BR. Target mechanism of iturinic lipopeptide on differential expression patterns of defense-related genes against Colletotrichum acutatum in Pepper. Plants, 2022, 11: 1267

[98] Dunlap, C. A., Bowman, M. J., Rooney, A. P. Iturinic lipopeptide diversity in the bacillus subtilis species group—important antifungals for plant disease biocontrol applications. Front. Microbiol. 2019;10.

[99] Malviya D et al. Lesson from ecotoxicity: revisiting the microbial lipopeptides for the management of emerging diseases for crop protection. Int. J. Environ. Res. Public Health, 2020, 17: 1434

[100] Serino L et al. Biosynthesis of pyochelin and dihydroaeruginoic acid requires the iron-regulated pchDCBA operon in Pseudomonas aeruginosa. J. Bacteriol., 1997, 179: 248-257

[101] Kerr JR et al. Pseudomonas aeruginosa pyocyanin and 1-hydroxyphenazine inhibit fungal growth. J. Clin. Pathol., 1999, 52: 385-387

[102] Greber EK, Dawgul M. Antimicrobial peptides under clinical trials. Curr. Top. Med. Chem., 2016, 17: 620-628

[103] de Breij A et al. The antimicrobial peptide SAAP-148 combats drug-resistant bacteria and biofilms. Sci. Transl. Med, 2018, 10: eaan4044

[104] Teeri AE, Josselyn D. Effect of excess amino acids on growth of certain lactobacilli. J. Bacteriol., 1953, 66: 72-73

[105] Graham C et al. Studies on natural and racemic amino acids with rats. J. Biol. Chem., 1950, 185: 97-102

[106] Espaillat A et al. Structural basis for the broad specificity of a new family of amino-acid racemases. Acta Crystallogr. Sect. D. Biol. Crystallogr., 2014, 70: 79-90

[107] Hernández SB, Cava F. Environmental roles of microbial amino acid racemases. Environ. Microbiol., 2016, 18: 1673-1685

[108] Aliashkevich, A., Alvarez, L., Cava, F. New insights into the mechanisms and biological roles of d-amino acids in complex eco-systems. Front. Microbiol. 9, 683 (2018).

[109] Radkov AD, Moe LA. Bacterial synthesis of d-amino acids. Appl. Microbiol. Biotechnol., 2014, 98: 5363-5374

[110] Mutaguchi Y, Ohmori T, Wakamatsu T, Doi K, Ohshima T. Identification, purification, and characterization of a novel amino acid racemase, isoleucine 2-epimerase, from Lactobacillus species. J. Bacteriol., 2013, 195: 5207-5215

[111] Yoshimura T, Esak N. Amino acid racemases: functions and mechanisms. J. Biosci. Bioeng., 2003, 96: 103-109

[112] Cava F, Lam H, de Pedro MA, Waldor MK. Emerging knowledge of regulatory roles of d-amino acids in bacteria. Cell Mol. Life Sci., 2011, 68: 817-831

[113] Lam H et al. D-Amino acids govern stationary phase cell wall remodeling in bacteria. Science, 2009, 325: 1552-1555

[114] Ogasawara, Y., Dairi, T. Peptide epimerization machineries found in microorganisms. Front. Microbiol. 9, 156 (2018).

[115] Fischer C, Ahn Y-C, Vederas JC. Catalytic mechanism and properties of pyridoxal 5′-phosphate independent racemases: how enzymes alter mismatched acidity and basicity. Nat. Prod. Rep., 2019, 36: 1687-1705

[116] Gao X, Ma Q, Zhu H. Distribution, industrial applications, and enzymatic synthesis of d-amino acids. Appl. Microbiol. Biotechnol., 2015, 99: 3341-3349

[117] Bucher T, Oppenheimer-Shaanan Y, Savidor A, Bloom-Ackermann Z, Kolodkin-Gal I. Disturbance of the bacterial cell wall specifically interferes with biofilm formation. Environ. Microbiol. Rep., 2015, 7: 990-1004

[118] Kolodkin-Gal I et al. d-Amino acids trigger biofilm disassembly. Science, 2010, 328: 627-629

[119] Vollmer W, Blanot D, De Pedro MA. Peptidoglycan structure and architecture. FEMS Microbiol. Rev., 2008, 32: 149-167

[120] Young KD. The selective value of bacterial shape. Microbiol. Mol. Biol. Rev., 2006, 70: 660-703

[121] Pollegioni L, Molla G. The conundrum in enzymatic reactions related to biosynthesis of d‐amino acids in bacteria. FEBS J., 2022, 289: 5895-5898

[122] Hsu Y-P, Booher G, Egan A, Vollmer W, VanNieuwenhze MS. d-Amino acid derivatives as in situ probes for visualizing bacterial peptidoglycan biosynthesis. Acc. Chem. Res., 2019, 52: 2713-2722

[123] Dramsi S, Magnet S, Davison S, Arthur M. Covalent attachment of proteins to peptidoglycan. FEMS Microbiol. Rev., 2008, 32: 307-320

[124] Bellais S et al. Aslfm, the D-aspartate ligase responsible for the addition of D-aspartic acid onto the peptidoglycan precursor of Enterococcus faecium. J. Biol. Chem., 2006, 281: 11586-11594

[125] Sieradzki K. A highly vancomycin-resistant laboratory mutant of Staphylococcus aureus. FEMS Microbiol. Lett., 1996, 142: 161-166

[126] Veiga P et al. Identification of an essential gene responsible for d-Asp incorporation in the Lactococcus lactis peptidoglycan crossbridge. Mol. Microbiol, 2006, 62: 1713-1724

[127] Reynolds PE, Courvalin P. Vancomycin resistance in Enterococci due to synthesis of precursors terminating in d-Alanyl- d-Serine. Antimicrob. Agents Chemother., 2005, 49: 21-25

[128] Cava F, de Pedro MA, Lam H, Davis BM, Waldor MK. Distinct pathways for modification of the bacterial cell wall by non-canonical D-amino acids. EMBO J., 2011, 30: 3442-3453

[129] Wang Q et al. In vitro and in vivo activity of d-serine in combination with β-lactam antibiotics against methicillin-resistant Staphylococcus aureus. Acta Pharm. Sin. B, 2019, 9: 496-504

[130] Tremp M et al. Clostridial infection after open fractures of the lower extremity – report of two cases and discussion of pathomechanism and treatment. In Vivo, 2020, 34: 291-298

[131] Stroud G, Vandiver JW. Clostridium perfringens as an unusual cause of a prosthetic joint infection following total knee arthroplasty. IDCases, 2020, 20: e00789

[132] Tehri N, Kumar N, Raghu H, Vashishth A. Biomarkers of bacterial spore germination. Ann. Microbiol., 2018, 68: 513-523

[133] Tehri N, Kumar N, Yadav A, Raghu HV, Singh NA. Sugars mediated germination in spores of Bacillus megaterium. Int. J. Microbiol. Res., 2018, 10: 1058

[134] Tennen R, Setlow B, Davis KL, Loshon CA, Setlow P. Mechanisms of killing of spores of Bacillus subtilis by iodine, glutaraldehyde and nitrous acid. J. Appl Microbiol, 2000, 89: 330-338

[135] Atluri S, Ragkousi K, Cortezzo DE, Setlow P. Cooperativity between different nutrient receptors in germination of spores of Bacillus subtilis and reduction of this cooperativity by alterations in the GerB Receptor. J. Bacteriol., 2006, 188: 28-36

[136] Chesnokova ON, McPherson SA, Steichen CT, Turnbough CL. The spore-specific alanine racemase of Bacillus anthracis and its role in suppressing germination during spore development. J. Bacteriol., 2009, 191: 1303-1310

[137] McKevitt MT et al. Effects of endogenous d-alanine synthesis and autoinhibition of bacillus anthracis germination on in vitro and in vivo infections. Infect. Immun., 2007, 75: 5726-5734

[138] Hu H, Emerson J, Aronson AI. Factors involved in the germination and inactivation of Bacillus anthracis spores in murine primary macrophages. FEMS Microbiol. Lett., 2007, 272: 245-250

[139] Hood MI, Skaar EP. Nutritional immunity: transition metals at the pathogen–host interface. Nat. Rev. Microbiol., 2012, 10: 525-537

[140] Corbin BD et al. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science, 2008, 319: 962-965

[141] Hennigar SR, McClung JP. Nutritional immunity. Am. J. Lifestyle Med., 2016, 10: 170-173

[142] Murdoch CC, Skaar EP. Nutritional immunity: the battle for nutrient metals at the host–pathogen interface. Nat. Rev. Microbiol., 2022, 20: 657-670

[143] Ghssein G et al. Biosynthesis of a broad-spectrum nicotianamine-like metallophore in Staphylococcus aureus. Science, 2016, 352: 1105-1109

[144] Anfora AT, Haugen BJ, Roesch P, Redford P, Welch RA. Roles of serine accumulation and catabolism in the colonization of the murine urinary tract by Escherichia coli CFT073. Infect. Immun., 2007, 75: 5298-5304

[145] Connolly JP et al. The host metabolite D-serine contributes to bacterial niche specificity through gene selection. ISME J., 2015, 9: 1039-1051

[146] O’Boyle N, Roe AJ. Heterogeneity in populations of enterohaemorrhagic Escherichia coli undergoing d-serine adaptation. Curr. Genet., 2021, 67: 221-224

[147] Lee, R. J. et al. Bacterial d-amino acids suppress sinonasal innate immunity through sweet taste receptors in solitary chemosensory cells. Sci. Signal. 10, eaam7703 (2017).

[148] Tecle T, Tripathi S, Hartshorn KL. Review: defensins and cathelicidins in lung immunity. Innate Immun., 2010, 16: 151-159

[149] Lee RJ et al. Bitter and sweet taste receptors regulate human upper respiratory innate immunity. J. Clin. Investig., 2014, 124: 1393-1405

[150] Kepert I et al. D-tryptophan from probiotic bacteria influences the gut microbiome and allergic airway disease. J. Allergy Clin. Immunol., 2017, 139: 1525-1535

[151] An YH, Friedman RJ. Concise review of mechanisms of bacterial adhesion to biomaterial surfaces. J. Biomed. Mater. Res., 1998, 43: 338-348

[152] Katsikogianni M, Missirlis Y. Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria-material interactions. Eur. Cells Mater., 2004, 8: 37-57

[153] Kline KA, Fälker S, Dahlberg S, Normark S, Henriques-Normark B. Bacterial adhesins in host-microbe interactions. Cell Host Microbe, 2009, 5: 580-592

[154] Ishihama H et al. An antibacterial coated polymer prevents biofilm formation and implant-associated infection. Sci. Rep., 2021, 11

[155] Teughels W, Van Assche N, Sliepen I, Quirynen M. Effect of material characteristics and/or surface topography on biofilm development. Clin. Oral. Implants Res., 2006, 17 S2 68-81

[156] Katainen J, Paajanen M, Ahtola E, Pore V, Lahtinen J. Adhesion as an interplay between particle size and surface roughness. J. Colloid Interface Sci., 2006, 304: 524-529

[157] Truong VK et al. The influence of nano-scale surface roughness on bacterial adhesion to ultrafine-grained titanium. Biomaterials, 2010, 31: 3674-3683

[158] Whitehead KA, Colligon J, Verran J. Retention of microbial cells in substratum surface features of micrometer and sub-micrometer dimensions. Colloids Surf. B Biointerfaces, 2005, 41: 129-138

[159] Webster TJ, Tong Z, Liu J, Banks MK. Adhesion of Pseudomonas fluorescens onto nanophase materials. Nanotechnology, 2005, 16: S449-S457

[160] Colon G, Ward BC, Webster TJ. Increased osteoblast and decreasedStaphylococcus epidermidis functions on nanophase ZnO and TiO2. J. Biomed. Mater. Res. Part A, 2006, 78A: 595-604

[161] Merritt K, Shafer JW, Brown SA. Implant site infection rates with porous and dense materials. J. Biomed. Mater. Res., 1979, 13: 101-108

[162] Khatoon Z, McTiernan CD, Suuronen EJ, Mah T-F, Alarcon EI. Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon, 2018, 4: e01067

[163] Wolden R et al. Identification of surface proteins in a clinical Staphylococcus haemolyticus isolate by bacterial surface shaving. BMC Microbiol., 2020, 20: 80

[164] Campoccia D et al. Orthopedic implant infections: Incompetence of Staphylococcus epidermidis, Staphylococcus lugdunensis, and Enterococcus faecalis to invade osteoblasts. J. Biomed. Mater. Res. Part A, 2016, 104: 788-801

[165] Kubica M et al. A potential new pathway for staphylococcus aureus dissemination: the silent survival of S. aureus phagocytosed by human monocyte-derived macrophages. PLoS One, 2008, 3: e1409

[166] Wen Q, Gu F, Sui Z, Su Z, Yu T. The process of osteoblastic infection by Staphylococcus Aureus. Int. J. Med. Sci., 2020, 17: 1327-1332

[167] Proctor RA et al. Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat. Rev. Microbiol., 2006, 4: 295-305

[168] Bui LMG, Conlon BP, Kidd SP. Antibiotic tolerance and the alternative lifestyles of Staphylococcus aureus. Essays Biochem., 2017, 61: 71-79

[169] Hochbaum AI et al. Inhibitory effects of d-amino acids on staphylococcus aureus biofilm development. J. Bacteriol., 2011, 193: 5616-5622

[170] Xing S-F et al. D-Amino acids inhibit initial bacterial adhesion: thermodynamic evidence. Biotechnol. Bioeng., 2015, 112: 696-704

[171] Yu C et al. Inhibition of biofilm formation by d-tyrosine: effect of bacterial type and d-tyrosine concentration. Water Res., 2016, 92: 173-179

[172] Su X, Cheng X, Wang Y, Luo J. Effect of different D-amino acids on biofilm formation of mixed microorganisms. Water Sci. Technol., 2022, 85: 116-124

[173] Xu H, Liu Y. Reduced microbial attachment by d-amino acid-inhibited AI-2 and EPS production. Water Res., 2011, 45: 5796-5804

[174] Rumbo C et al. Assessment of antivirulence activity of several d-amino acids against Acinetobacter baumannii and Pseudomonas aeruginosa. J. Antimicrob. Chemother., 2016, 71: 3473-3481

[175] Lupoli TJ et al. Transpeptidase-mediated incorporation of d-amino acids into bacterial peptidoglycan. J. Am. Chem. Soc., 2011, 133: 10748-10751

[176] Gupta P, Sarkar S, Das B, Bhattacharjee S, Tribedi P. Biofilm, pathogenesis and prevention—a journey to break the wall: a review. Arch. Microbiol., 2016, 198: 1-15

[177] Wu H, Moser C, Wang H-Z, Høiby N, Song Z-J. Strategies for combating bacterial biofilm infections. Int. J. Oral. Sci., 2015, 7: 1-7

[178] Davey ME, O’toole GA. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev., 2000, 64: 847-867

[179] Wildeman P et al. Genomic characterization and outcome of prosthetic joint infections caused by Staphylococcus aureus. Sci. Rep., 2020, 10

[180] Corvec S, Portillo ME, Pasticci BM, Borens O, Trampuz A. Epidemiology and new developments in the diagnosis of prosthetic joint infection. Int. J. Artif. Organs, 2012, 35: 923-934

[181] Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW. Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials, 2012, 33: 5967-5982

[182] Brady RA, Leid JG, Calhoun JH, Costerton JW, Shirtliff ME. Osteomyelitis and the role of biofilms in chronic infection. FEMS Immunol. Med. Microbiol, 2008, 52: 13-22

[183] Suligoy, C. M. et al. Mutation of Agr is associated with the adaptation of Staphylococcus aureus to the Host during Chronic Osteomyelitis. Front. Cell Infect. Microbiol. 8, 18 (2018).

[184] Sanchez CJ et al. Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect. Dis., 2013, 13

[185] Junka A et al. Bad to the bone: on in vitro and ex vivo microbial biofilm ability to directly destroy colonized bone surfaces without participation of host immunity or osteoclastogenesis. PLoS One, 2017, 12: e0169565

[186] Lister JL, Horswill AR. Staphylococcus aureus biofilms: recent developments in biofilm dispersal. Front. Cell Infect. Microbiol, 2014, 4: 178

[187] Archer NK et al. Staphylococcus aureus biofilms. Virulence, 2011, 2: 445-459

[188] Beenken KE et al. Epistatic relationships between sarA and agr in Staphylococcus aureus biofilm formation. PLoS One, 2010, 5: e10790

[189] Cucarella C et al. a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol., 2001, 183: 2888-2896

[190] Geoghegan JA et al. Role of surface protein SasG in biofilm formation by Staphylococcus aureus. J. Bacteriol., 2010, 192: 5663-5673

[191] O’Neill E et al. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J. Bacteriol., 2008, 190: 3835-3850

[192] Schroeder K et al. Molecular characterization of a novel Staphylococcus aureus surface protein (SasC) involved in cell aggregation and biofilm accumulation. PLoS One, 2009, 4: e7567

[193] Sarkar S, Pires MM. d-Amino acids do not inhibit biofilm formation in Staphylococcus aureus. PLoS One, 2015, 10: e0117613

[194] Sanchez CJ et al. Effects of local delivery of d-amino acids from biofilm-dispersive scaffolds on infection in contaminated rat segmental defects. Biomaterials, 2013, 34: 7533-7543

[195] Harmata AJ et al. d-Amino acid inhibits biofilm but not new bone formation in an ovine model. Clin. Orthop. Relat. Res., 2015, 473: 3951-3961

[196] Li Y et al. Effects of intra-articular D-amino acids combined with systemic vancomycin on an experimental Staphylococcus aureus-induced periprosthetic joint infection. J. Microbiol. Immunol. Infect., 2022, 55: 716-727

[197] Sanchez CJ et al. d-Amino acids enhance the activity of antimicrobials against biofilms of clinical wound isolates of Staphylococcus aureus and Pseudomonas aeruginosa. Antimicrob. Agents Chemother., 2014, 58: 4353-4361

[198] Yang, H., Wang, M., Yu, J. & Wei, H. Aspartate inhibits Staphylococcus aureus biofilm formation. FEMS Microbiol, Lett. 362, fnv025 (2015).

[199] Wickramasinghe S et al. Photoactivated gold nanorod hydrogel composite containing d-amino acids for the complete eradication of bacterial biofilms on metal alloy implant materials. ACS Appl Nano Mater., 2020, 3: 5862-5873

[200] Xu Z et al. Whole genome sequence and comparative genomics analysis of multi-drug resistant environmental Staphylococcus epidermidis ST59. G3 Genes|Genomes|Genet., 2018, 8: 2225-2230

[201] Arciola CR et al. Antibiotic resistance in exopolysaccharide-forming Staphylococcus epidermidis clinical isolates from orthopaedic implant infections. Biomaterials, 2005, 26: 6530-6535

[202] Fey PD, Olson ME. Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiol., 2010, 5: 917-933

[203] Rohde H et al. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol. Microbiol., 2005, 55: 1883-1895

[204] Vuong C, Kocianova S, Yao Y, Carmody AB, Otto M. Increased colonization of indwelling medical devices by quorum‐sensing mutants of Staphylococcus epidermidis in vivo. J. Infect. Dis., 2004, 190: 1498-1505

[205] Ramón-Peréz ML et al. D-Amino acids inhibit biofilm formation in Staphylococcus epidermidis strains from ocular infections. J. Med. Microbiol., 2014, 63: 1369-1376

[206] Ebert, S., Meier, C., Meili, S., Wahl, P. Lessons learned from an implant-related infection with bacillus spp of the proximal femur: a rare and insidious complication after internal fixation of closed fractures. Biomed. J. Sci. Technol. Res. 19. https://doi.org/10.26717/BJSTR.2019.19.003274 (2019).

[207] Dubouix A et al. Bacillus cereus infections in Traumatology–Orthopaedics Department: retrospective investigation and improvement of healthcare practices. J. Infect., 2005, 50: 22-30

[208] Gallo PH et al. Demonstration of Bacillus cereus in orthopaedic-implant-related infection with use of a multi-primer polymerase chain reaction-mass spectrometric assay. J. Bone Jt Surg., 2011, 93: e85

[209] Ha J, Park YJ, Kim YJ, Oh HC, Kim YA. Late prosthetic joint infection and bacteremia by Bacillus cereus confirmed by 16S rRNA sequencing and hip joint tissue pathology. Ann. Clin. Microbiol, 2016, 19: 54

[210] Mitton, B., Rule, R., Mbelle, N., van Hougenhouck-Tulleken, W., Said, M. Post-procedural Bacillus cereus septic arthritis in a patient with systemic lupus erythematosus. Afr. J. Lab. Med. 9, 1119 (2020).

[211] Wiedermann CJ, Stockner I, Plattner B. Bacillus species infective arthritis after knee arthroscopy. Surg. Infect., 2010, 11: 555-558

[212] Romero D, Aguilar C, Losick R, Kolter R. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc. Natl. Acad. Sci., 2010, 107: 2230-2234

[213] Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. Sticking together: building a biofilm the Bacillus subtilis way. Nat. Rev. Microbiol, 2013, 11: 157-168

[214] Kobayashi K, Iwano M. BslA(YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol. Microbiol., 2012, 85: 51-66

[215] Romero D, Vlamakis H, Losick R, Kolter R. An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol. Microbiol., 2011, 80: 1155-1168

[216] Kearns DB, Chu F, Branda SS, Kolter R, Losick R. A master regulator for biofilm formation by Bacillus subtilis. Mol. Microbiol., 2004, 55: 739-749

[217] Branda SS et al. Genes involved in formation of structured multicellular communities by Bacillus subtilis. J. Bacteriol., 2004, 186: 3970-3979

[218] Cámara-Almirón J et al. Dual functionality of the amyloid protein TasA in Bacillus physiology and fitness on the phylloplane. Nat. Commun., 2020, 11

[219] Leiman SA et al. D-Amino acids indirectly inhibit biofilm formation in bacillus subtilis by interfering with protein synthesis. J. Bacteriol., 2013, 195: 5391-5395

[220] Sonohata M, Kitajima M, Kawano S, Mawatari M. Acute hematogenous infection of revision total hip arthroplasty by oral bacteria in a patient without a history of dental procedures: case report. Open Orthop. J., 2014, 8: 56-59

[221] Olson LB, Turner DJ, Cox GM, Hostler CJ. Streptococcus salivarius prosthetic joint infection following dental cleaning despite antibiotic prophylaxis. Case Rep. Infect. Dis., 2019, 2019: 1-4

[222] Friedlander AH. Presence of staphylococci in mouth and presence of streptococci in late infections of knee and hip joint prostheses: antibiotic prophylaxis, a conundrum. Spec. Care Dent., 2009, 29: 226-228

[223] Mathur A, Chen AF. Streptococcus viridans periprosthetic joint infections. Ann. Jt, 2017, 2: 36-36

[224] Takahashi N, Nyvad B. The role of bacteria in the caries process. J. Dent. Res., 2011, 90: 294-303

[225] Koo H, Falsetta ML, Klein MI. The exopolysaccharide matrix. J. Dent. Res., 2013, 92: 1065-1073

[226] Lemos, J. A., et al. The biology of Streptococcus mutans. Microbiol. Spectr. 7. https://doi.org/10.1128/microbiolspec.GPP3-0051-2018 (2019).

[227] Bowen WH, Koo H. Biology of <i>Streptococcus mutans-</i>derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res, 2011, 45: 69-86

[228] Brady LJ et al. The changing faces of Streptococcus antigen I/II polypeptide family adhesins. Mol. Microbiol., 2010, 77: 276-286

[229] Tong Z et al. An in vitro study on the effect of free amino acids alone or in combination with Nisin on biofilms as well as on planktonic bacteria of Streptococcus mutans. PLoS One, 2014, 9: e99513

[230] Rasouli MR et al. Low rate of infection control in enterococcal periprosthetic joint infections. Clin. Orthop. Relat. Res., 2012, 470: 2708-2716

[231] Fernandes A. The microbiological profiles of infected prosthetic implants with an emphasis on the organisms which form biofilms. J Clin DIAGNOSTIC Res, 2013, 7: 219-223

[232] Osmon DR et al. Diagnosis and management of prosthetic joint infection: clinical practice guidelines by the Infectious Diseases Society of Americaa. Clin. Infect. Dis., 2013, 56: e1-e25

[233] Tornero E et al. Characteristics of prosthetic joint infections due to Enterococcus sp. and predictors of failure: a multi-national study. Clin. Microbiol. Infect., 2014, 20: 1219-1224

[234] Sandoe JAT, Wysome J, West AP, Heritage J, Wilcox MH. Measurement of ampicillin, vancomycin, linezolid and gentamicin activity against enterococcal biofilms. J. Antimicrob. Chemother., 2006, 57: 767-770

[235] Renz N, Trebse R, Akgün D, Perka C, Trampuz A. Enterococcal periprosthetic joint infection: clinical and microbiological findings from an 8-year retrospective cohort study. BMC Infect. Dis., 2019, 19

[236] Thompson O, Rasmussen M, Stefánsdóttir A, Christensson B, Åkesson P. A population-based study on the treatment and outcome of enterococcal prosthetic joint infections. A consecutive series of 55 cases. J. Bone Jt. Infect., 2019, 4: 285-291

[237] Holmberg A, Thórhallsdóttir VG, Robertsson O, W-Dahl A, Stefánsdóttir A. 75% success rate after open debridement, exchange of tibial insert, and antibiotics in knee prosthetic joint infections. Acta Orthop., 2015, 86: 457-462

[238] Lam A, Rasmussen M, Thompson O. Successful outcome for patients with streptococcal prosthetic joint infections—a retrospective population-based study. Infect. Dis., 2018, 50: 593-600

[239] Paganelli FL, Willems RJ, Leavis HL. Optimizing future treatment of enterococcal infections: attacking the biofilm. Trends Microbiol., 2012, 20: 40-49

[240] Zheng J et al. Characterization of biofilm formation by Enterococcus faecalis isolates derived from urinary tract infections in China. J. Med. Microbiol, 2018, 67: 60-67

[241] Kayaoglu G, Ørstavik DV. Crit. Rev. Oral. Biol. Med., 2004, 15: 308-320

[242] Park SY, Kim KM, Lee JH, Seo SJ, Lee IH. Extracellular gelatinase of Enterococcus faecalis destroys a defense system in insect hemolymph and human serum. Infect. Immun., 2007, 75: 1861-1869

[243] Chuang-Smith ON, Wells CL, Henry-Stanley MJ, Dunny GM. Acceleration of Enterococcus faecalis biofilm formation by aggregation substance expression in an ex vivo model of cardiac valve colonization. PLoS One, 2010, 5: e15798

[244] Afonina I, Lim XN, Tan R, Kline KA. Planktonic Interference and Biofilm Alliance between Aggregation Substance and Endocarditis- and Biofilm-Associated Pili in Enterococcus faecalis. J. Bacteriol, 2018, 200: e00361-18

[245] Zilm PS et al. D-amino acids reduce Enterococcus faecalis biofilms in vitro and in the presence of antimicrobials used for root canal treatment. PLoS One, 2017, 12: e0170670

[246] Rosen, E., Tsesis, I., Elbahary, S., Storzi, N., Kolodkin-Gal, I. Eradication of Enterococcus faecalis biofilms on human dentin. Front. Microbiol. 7, 2055 (2016).

[247] Pestrak MJ et al. Pseudomonas aeruginosa rugose small-colony variants evade host clearance, are hyper-inflammatory, and persist in multiple host environments. PLOS Pathog., 2018, 14: e1006842

[248] Cerioli M et al. Pseudomonas aeruginosa implant-associated bone and joint infections: experience in a regional reference center in France. Front. Med, 2020, 7: 513242

[249] Seyman D, Ozen NS, Inan D, Ongut G, Ogunc D. Pseudomonas aeruginosa septic arthritis of knee after intra-articular ozone injection. N. Microbiol., 2012, 35: 345-348

[250] Yilmaz M, Arslan F, Mert A. Community acquired chronic arthritis due to Pseudomonas aeruginosa in a previously healthy pregnant woman. Case Rep. Infect. Dis., 2014, 2014: 1-2

[251] Sudduth JD et al. Open fractures: are we still treating the same types of infections. Surg. Infect., 2020, 21: 766-772

[252] Triffault-Fillit C et al. Microbiologic epidemiology depending on time to occurrence of prosthetic joint infection: a prospective cohort study. Clin. Microbiol. Infect., 2019, 25: 353-358

[253] Lora-Tamayo J et al. Infected hip hemiarthroplasties and total hip arthroplasties: differential findings and prognosis. J. Infect., 2013, 67: 536-544

[254] Ascione T et al. Factors related to outcome of early and delayed prosthetic joint infections. J. Infect., 2015, 70: 30-36

[255] Veltman ES, Vos FJ, Meis JF, Goosen JHM. Debridement, antibiotics and implant retention in early postoperative infection with Pseudomonas aeruginosa. J. Infect., 2015, 70: 307-309

[256] Semmler ABT, Whitchurch CB, Mattick JS. A re-examination of twitching motility in Pseudomonas aeruginosa. Microbiology, 1999, 145: 2863-2873

[257] Thi MTT, Wibowo D, Rehm BHA. Pseudomonas aeruginosa bbiofilms. Int. J. Mol. Sci., 2020, 21: 8671

[258] Chang C-Y. Surface sensing for biofilm formation in Pseudomonas aeruginosa. Front. Microbiol, 2018, 8: 2671

[259] Colvin KM et al. The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ. Microbiol., 2012, 14: 1913-1928

[260] Colvin KM et al. The pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PLoS Pathog., 2011, 7: e1001264

[261] Kao WTK, Frye M, Gagnon P, Vogel JP, Chole R. D-amino acids do not inhibit Pseudomonas aeruginosa biofilm formation. Laryngosc. Investig. Otolaryngol., 2017, 2: 4-9

[262] He W, Li C, Lu C-D. Regulation and characterization of the dadRAX Locus for d-amino acid catabolism in Pseudomonas aeruginosa PAO1. J. Bacteriol., 2011, 193: 2107-2115

[263] Brandenburg KS et al. Tryptophan inhibits biofilm formation by Pseudomonas aeruginosa. Antimicrob. Agents Chemother., 2013, 57: 1921-1925

[264] Ruer S, Stender S, Filloux A, de Bentzmann S. Assembly of fimbrial structures in Pseudomonas aeruginosa: functionality and specificity of chaperone-usher machineries. J. Bacteriol., 2007, 189: 3547-3555

[265] Conrad JC et al. Flagella and pili-mediated near-surface single-cell motility mechanisms in P. aeruginosa. Biophys. J., 2011, 100: 1608-1616

[266] Seifert H et al. Distribution of Acinetobacter species on human skin: comparison of phenotypic and genotypic identification methods. J. Clin. Microbiol., 1997, 35: 2819-2825

[267] Colquhoun JM, Rather PN. Insights into mechanisms of biofilm formation in Acinetobacter baumannii and Implications for Uropathogenesis. Front. Cell.Infect. Microbiol, 2020, 10: 253

[268] Choe H et al. Staphylococcus aureus and Acinetobacter baumannii inhibit osseointegration of orthopedic implants. Infect. Immun, 2022, 90: e0066921

[269] Lob SH, Hoban DJ, Sahm DF, Badal RE. Regional differences and trends in antimicrobial susceptibility of Acinetobacter baumannii. Int. J. Antimicrob. Agents, 2016, 47: 317-323

[270] Giammanco A, Calà C, Fasciana T, Dowzicky MJ. Global assessment of the activity of tigecycline against multidrug-resistant gram-negative pathogens between 2004 and 2014 as part of the tigecycline evaluation and surveillance trial. mSphere, 2017, 2: e00310-16

[271] Ramirez MS, Bonomo RA, Tolmasky ME. Carbapenemases: transforming acinetobacter baumannii into a yet more dangerous menace. Biomolecules, 2020, 10: 720

[272] Benito N et al. The different microbial etiology of prosthetic joint infections according to route of acquisition and time after prosthesis implantation, including the role of multidrug-resistant organisms. J. Clin. Med., 2019, 8: 673

[273] Benito N et al. Time trends in the aetiology of prosthetic joint infections: a multicentre cohort study. Clin. Microbiol. Infect., 2016, 22: 732.e1-732.e8

[274] da Silva RB, Araujo RO, Salles MJ. Non-elective and revision arthroplasty are independently associated with hip and knee prosthetic joint infection caused by Acinetobacter baumannii: a Brazilian single center observational cohort study of 98 patients. BMC Musculoskelet. Disord., 2021, 22

[275] Silva R et al. Orthopedic-implant associated infection due to gram-negative bacilli: the worrisome impact of Acinetobacter baumannii multidrug resistance in a Brazilian center. Open Forum Infect. Dis., 2017, 4 suppl_1 S111-S112

[276] Johnson EN, Burns TC, Hayda RA, Hospenthal DR, Murray CK. Infectious complications of open type iii tibial fractures among combat casualties. Clin. Infect. Dis., 2007, 45: 409-415

[277] Fily F et al. Post-traumatic osteomyelitis in Middle East war-wounded civilians: resistance to first-line antibiotics in selected bacteria over the decade 2006–2016. BMC Infect. Dis., 2019, 19

[278] Petersen K et al. Trauma-related infections in battlefield casualties from Iraq. Ann. Surg., 2007, 245: 803-811

[279] De Gregorio E et al. Biofilm-associated proteins: news from Acinetobacter. BMC Genom., 2015, 16

[280] Jariyarattanarach P, Klubthawee N, Wongchai M, Roytrakul S, Aunpad R. Novel D-form of hybrid peptide (D-AP19) rapidly kills Acinetobacter baumannii while tolerating proteolytic enzymes. Sci. Rep., 2022, 12

[281] Sasabe J et al. Interplay between microbial d-amino acids and host d-amino acid oxidase modifies murine mucosal defence and gut microbiota. Nat. Microbiol., 2016, 1: 16125

[282] Kawase T et al. Gut microbiota of mice putatively modifies amino acid metabolism in the host brain. Br. J. Nutr., 2017, 117: 775-783

[283] Ding X, Ma N, Nagahama M, Yamada K, Semba R. Localization of d-serine and serine racemase in neurons and neuroglias in mouse brain. Neurol. Sci., 2011, 32: 263-267

[284] Kartvelishvily E, Shleper M, Balan L, Dumin E, Wolosker H. Neuron-derived D-serine release provides a novel means to activate N-methyl-D-aspartate receptors. J. Biol. Chem., 2006, 281: 14151-14162

[285] Williams SM, Diaz CM, Macnab LT, Sullivan RKP, Pow DV. Immunocytochemical analysis ofD-serine distribution in the mammalian brain reveals novel anatomical compartmentalizations in glia and neurons. Glia, 2006, 53: 401-411

[286] Kiriyama Y, Nochi H. D-Amino acids in the nervous and endocrine systems. Science, 2016, 2016: 1-9

[287] Beltrán-Castillo S et al. D-serine released by astrocytes in brainstem regulates breathing response to CO₂ levels. Nat. Commun., 2017, 8

[288] Beltrán-Castillo S, Eugenín J, von Bernhardi R. Impact of aging in microglia-mediated D-serine balance in the CNS. Mediators Inflamm., 2018, 2018: 1-11

[289] von Bernhardi R, Eugenín-von Bernhardi L, Eugenín J. Microglial cell dysregulation in brain aging and neurodegeneration. Front. Aging Neurosci, 2015, 7: 124

[290] Ollivaux C, Soyez D, Toullec J-Y. Biogenesis of d-amino acid containing peptides/proteins: where, when and how? J. Pept. Sci., 2014, 20: 595-612

[291] Madeira C et al. d-serine levels in Alzheimer’s disease: implications for novel biomarker development. Transl. Psychiatry, 2015, 5: e561-e561

[292] Lin C-H, Yang H-T, Chiu C-C, Lane H-Y. Blood levels of D-amino acid oxidase vs. D-amino acids in reflecting cognitive aging. Sci. Rep., 2017, 7

[293] Guercio, G. D., Panizzutti, R. Potential and challenges for the clinical use of d-serine as a cognitive enhancer. Front. Psychiatry. 9, 14 (2018).

[294] Klatte K et al. Impaired D-serine-mediated cotransmission mediates cognitive dysfunction in epilepsy. J. Neurosci., 2013, 33: 13066-13080

[295] Takarada T et al. Osteoclastogenesis is negatively regulated by D-serine produced by osteoblasts. J. Cell Physiol., 2012, 227: 3477-3487

[296] Rivera-Villaseñor A et al. NMDA receptor hypofunction in the aging-associated malfunction of peripheral tissue. Front. Physiol, 2021, 12: 687121

[297] D’Aniello S, Somorjai I, Garcia‐Fernàndez J, Topo E, D’Aniello A. D‐Aspartic acid is a novel endogenous neurotransmitter. FASEB J., 2011, 25: 1014-1027

[298] Errico F et al. A role for D-aspartate oxidase in schizophrenia and in schizophrenia-related symptoms induced by phencyclidine in mice. Transl. Psychiatry, 2015, 5: e512-e512

[299] Fujii N, Takata T, Fujii N, Aki K, Sakaue H. D-Amino acids in protein: the mirror of life as a molecular index of aging. Biochim. Biophys. Acta - Proteins Proteom., 2018, 1866: 840-847

[300] Patton A, Genever P, Birch M, Suva L, Skerry T. Expression of an N-methyl-D-aspartate-type receptor by human and rat osteoblasts and osteoclasts suggests a novel glutamate signaling pathway in bone. Bone, 1998, 22: 645-649

[301] Ho M-L et al. Down-regulation of N-methyl D-aspartate receptor in rat-modeled disuse osteopenia. Osteoporos. Int, 2005, 16: 1780-1788

[302] Cloos PAC, Fledelius C. Collagen fragments in urine derived from bone resorption are highly racemized and isomerized: a biological clock of protein aging with clinical potential. Biochem. J., 2000, 345: 473-480

[303] Fujii N et al. The presence of d-β-aspartic acid-containing peptides in elastic fibers of sun-damaged skin: a potent marker for ultraviolet-induced skin aging. Biochem. Biophys. Res. Commun., 2002, 294: 1047-1051

[304] Hooi MYS, Truscott RJW. Racemisation and human cataract. d-Ser, d-Asp/Asn and d-Thr are higher in the lifelong proteins of cataract lenses than in age-matched normal lenses. Age, 2011, 33: 131-141

[305] Nagata Y et al. High concentrations of D-amino acids in human gastric juice. Amino Acids, 2007, 32: 137-140

[306] Zhang Z et al. Non-invasive detection of gastric cancer relevant d-amino acids with luminescent DNA/silver nanoclusters. Nanoscale, 2017, 9: 19367-19373

[307] Han M et al. Development and validation of a rapid, selective, and sensitive LC–MS/MS method for simultaneous determination of d- and l-amino acids in human serum: application to the study of hepatocellular carcinoma. Anal. Bioanal. Chem., 2018, 410: 2517-2531

[308] Huang J-L, Chen X-L, Guo C, Wang Y-X. Contributions of spinal d-amino acid oxidase to bone cancer pain. Amino Acids, 2012, 43: 1905-1918

[309] Wang Y-X et al. Biological implications of oxidation and unidirectional chiral inversion of D-amino acids. Curr. Drug Metab., 2012, 13: 321-331

[310] Rosini E, Pollegioni L, Ghisla S, Orru R, Molla G. Optimization of d-amino acid oxidase for low substrate concentrations - towards a cancer enzyme therapy. FEBS J., 2009, 276: 4921-4932

[311] El Sayed SM et al. D-Amino acid oxidase-induced oxidative stress, 3-bromopyruvate and citrate inhibit angiogenesis, exhibiting potent anticancer effects. J. Bioenerg. Biomembr., 2012, 44: 513-523

[312] Bava A et al. D-amino acid oxidase–nanoparticle system: a potential novel approach for cancer enzymatic therapy. Nanomedicine, 2013, 8: 1797-1806

[313] Kimura T et al. Chiral amino acid metabolomics for novel biomarker screening in the prognosis of chronic kidney disease. Sci. Rep., 2016, 6

[314] Hesaka A et al. D-Serine reflects kidney function and diseases. Sci. Rep., 2019, 9

[315] Visser WF et al. A sensitive and simple ultra-high-performance-liquid chromatography–tandem mass spectrometry based method for the quantification of d-amino acids in body fluids. J. Chromatogr. A, 2011, 1218: 7130-7136

[316] Tsai GE, Yang P, Chang Y-C, Chong M-Y. D-Alanine added to antipsychotics for the treatment of schizophrenia. Biol. Psychiatry, 2006, 59: 230-234

[317] Tsai G, Yang P, Chung L-C, Lange N, Coyle JT. D-serine added to antipsychotics for the treatment of schizophrenia. Biol. Psychiatry, 1998, 44: 1081-1089

[318] Shi Y, Hussain Z, Zhao Y. Promising application of D-amino acids toward clinical therapy. Int. J. Mol. Sci., 2022, 23: 10794

[319] Rawson M, Haggard W, Jennings JA. Osteocompatibility of Biofilm Inhibitors. Open Orthop. J., 2014, 8: 442-449

[320] Ercal N, Luo X, Matthews RH, Armstrong DW. In vitro study of the metabolic effects of D-amino acids. Chirality, 1996, 8: 24-29

[321] Hsu Y-P et al. Full color palette of fluorescent d-amino acids for in situ labeling of bacterial cell walls. Chem. Sci., 2017, 8: 6313-6321

[322] Hsu Y-P et al. Fluorogenic d-amino acids enable real-time monitoring of peptidoglycan biosynthesis and high-throughput transpeptidation assays. Nat. Chem., 2019, 11: 335-341

[323] Kuru E, Tekkam S, Hall E, Brun YV, Van Nieuwenhze MS. Synthesis of fluorescent D-amino acids and their use for probing peptidoglycan synthesis and bacterial growth in situ. Nat. Protoc., 2015, 10: 33-52

[324] Neumann KD et al. Imaging active infection in vivo using D-amino acid derived PET radiotracers. Sci. Rep., 2017, 7

[325] Parker MFL et al. Sensing living bacteria in vivo using d-alanine-derived 11 C radiotracers. ACS Cent. Sci., 2020, 6: 155-165

[326] Ogawa K et al. Evaluation of Ga-DOTA-(D-Asp)n as bone imaging agents: D-aspartic acid peptides as carriers to bone. Sci. Rep., 2017, 7