Staphylococcus aureus and biofilms: transmission, threats, and promising strategies in animal husbandry.
Staphylococcus aureus
Animal husbandry
Biofilm
Mastitis
Mitigation strategies
Journal
Journal of animal science and biotechnology
ISSN: 1674-9782
Titre abrégé: J Anim Sci Biotechnol
Pays: England
ID NLM: 101581293
Informations de publication
Date de publication:
13 Mar 2024
13 Mar 2024
Historique:
received:
04
11
2023
accepted:
03
02
2024
medline:
13
3
2024
pubmed:
13
3
2024
entrez:
13
3
2024
Statut:
epublish
Résumé
Staphylococcus aureus (S. aureus) is a common pathogenic bacterium in animal husbandry that can cause diseases such as mastitis, skin infections, arthritis, and other ailments. The formation of biofilms threatens and exacerbates S. aureus infection by allowing the bacteria to adhere to pathological areas and livestock product surfaces, thus triggering animal health crises and safety issues with livestock products. To solve this problem, in this review, we provide a brief overview of the harm caused by S. aureus and its biofilms on livestock and animal byproducts (meat and dairy products). We also describe the ways in which S. aureus spreads in animals and the threats it poses to the livestock industry. The processes and molecular mechanisms involved in biofilm formation are then explained. Finally, we discuss strategies for the removal and eradication of S. aureus and biofilms in animal husbandry, including the use of antimicrobial peptides, plant extracts, nanoparticles, phages, and antibodies. These strategies to reduce the spread of S. aureus in animal husbandry help maintain livestock health and improve productivity to ensure the ecologically sustainable development of animal husbandry and the safety of livestock products.
Identifiants
pubmed: 38475886
doi: 10.1186/s40104-024-01007-6
pii: 10.1186/s40104-024-01007-6
doi:
Types de publication
Journal Article
Review
Langues
eng
Pagination
44Subventions
Organisme : National Key R&D Program of China
ID : 2022YFD1300404
Organisme : National Natural Science Foundation of China
ID : 31930106
Organisme : National Natural Science Foundation of China
ID : U23A20232
Organisme : National Natural Science Foundation of China
ID : U22A20514
Organisme : 2115 Talent Development Program of China Agricultural University
ID : 1041-00109019
Organisme : Pinduoduo-China Agricultural University Research Fund
ID : PC2023A01001
Organisme : Special Fund for Henan Agriculture Research System
ID : HARS-22-13-Z1
Informations de copyright
© 2024. The Author(s).
Références
Khairullah AR, Kurniawan SC, Effendi MH, Sudjarwo SA, Ramandinianto SC, Widodo A, et al. A review of new emerging livestock-associated methicillin-resistant Staphylococcus aureus from pig farms. Vet World. 2023;16(1):46–58. https://doi.org/10.14202/vetworld.2023.46-58 .
doi: 10.14202/vetworld.2023.46-58
pubmed: 36855358
pmcid: 9967705
Baker PH, Enger KM, Jacobi SK, Akers RM, Enger BD. Cellular proliferation and apoptosis in Staphylococcus aureus-infected heifer mammary glands experiencing rapid mammary gland growth. J Dairy Sci. 2023;106(4):2642–50. https://doi.org/10.3168/jds.2022-22716 .
doi: 10.3168/jds.2022-22716
pubmed: 36823008
Szafraniec GM, Szeleszczuk P, Dolka B. Review on skeletal disorders caused by Staphylococcus spp. in poultry. Vet Q. 2022;42(1):21–40. https://doi.org/10.1080/01652176.2022.2033880 .
doi: 10.1080/01652176.2022.2033880
pubmed: 35076352
pmcid: 8843168
Patel K, Godden SM, Royster E, Crooker BA, Timmerman J, Fox L. Relationships among bedding materials, bedding bacteria counts, udder hygiene, milk quality, and udder health in US dairy herds. J Dairy Sci. 2019;102(11):10213–34. https://doi.org/10.3168/jds.2019-16692 .
doi: 10.3168/jds.2019-16692
pubmed: 31447166
Gelasakis AI, Angelidis AS, Giannakou R, Filioussis G, Kalamaki MS, Arsenos G. Bacterial subclinical mastitis and its effect on milk yield in low-input dairy goat herds. J Dairy Sci. 2016;99(5):3698–708. https://doi.org/10.3168/jds.2015-10694 .
doi: 10.3168/jds.2015-10694
pubmed: 26898280
Guerrero I, Ferrian S, Penadés M, García-Quirós A, Pascual JJ, Selva L, et al. Host responses associated with chronic staphylococcal mastitis in rabbits. Vet J. 2015;204(3):338–44. https://doi.org/10.1016/j.tvjl.2015.03.020 .
doi: 10.1016/j.tvjl.2015.03.020
pubmed: 25951985
Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358(9276):135–8. https://doi.org/10.1016/s0140-6736(01)05321-1 .
doi: 10.1016/s0140-6736(01)05321-1
pubmed: 11463434
Nero LA, Botelho CV, Sovinski ÂI, Grossi JL, Call DR, Dos Santos BL. Occurrence and distribution of antibiotic-resistant Staphylococcus aureus in a Brazilian pork production Chain. J Food Prot. 2022;85(6):973–9. https://doi.org/10.4315/jfp-21-378 .
doi: 10.4315/jfp-21-378
pubmed: 35358316
Calabrese C, Seccia V, Pelaia C, Spinelli F, Morini P, Rizzi A, et al. S. aureus and IgE-mediated diseases: pilot or copilot? A narrative review. Expert Rev Clin Immunol. 2022;18(6):639–47. https://doi.org/10.1080/1744666X.2022.2074402 .
doi: 10.1080/1744666X.2022.2074402
pubmed: 35507006
Suzuki Y, Ono HK, Shimojima Y, Kubota H, Kato R, Kakuda T, et al. A novel staphylococcal enterotoxin SE02 involved in a staphylococcal food poisoning outbreak that occurred in Tokyo in 2004. Food Microbiol. 2020;92:103588. https://doi.org/10.1016/j.fm.2020.103588 .
doi: 10.1016/j.fm.2020.103588
pubmed: 32950172
Liu C, Ma N, Feng Y, Zhou M, Li H, Zhang X, et al. From probiotics to postbiotics: concepts and applications. AROH. 2023;1(1):92–114. https://doi.org/10.1002/aro2.7 .
doi: 10.1002/aro2.7
Tomao P, Pirolo M, Agnoletti F, Pantosti A, Battisti A, Di Martino G, et al. Molecular epidemiology of methicillin-resistant Staphylococcus aureus from dairy farms in North-eastern Italy. Int J Food Microbiol. 2020;332:108817. https://doi.org/10.1016/j.ijfoodmicro.2020.108817 .
doi: 10.1016/j.ijfoodmicro.2020.108817
pubmed: 32777624
Ma N, Chen X, Johnston LJ, Ma X. Gut microbiota‐stem cell niche crosstalk: A new territory for maintaining intestinal homeostasis. iMeta. 2022;1(4):e54. https://doi.org/10.1002/imt2.54 .
doi: 10.1002/imt2.54
Hancock REW, Alford MA, Haney EF. Antibiofilm activity of host defence peptides: complexity provides opportunities. Nat Rev Microbiol. 2021;19(12):786–97. https://doi.org/10.1038/s41579-021-00585-w .
doi: 10.1038/s41579-021-00585-w
pubmed: 34183822
da Silva BD, Bernardes PC, Pinheiro PF, Fantuzzi E, Roberto CD. Chemical composition, extraction sources and action mechanisms of essential oils: Natural preservative and limitations of use in meat products. Meat Sci. 2021;176:108463. https://doi.org/10.1016/j.meatsci.2021.108463 .
doi: 10.1016/j.meatsci.2021.108463
pubmed: 33640647
Broens EM, Graat EA, van de Giessen AW, Broekhuizen-Stins MJ, de Jong MC. Quantification of transmission of livestock-associated methicillin resistant Staphylococcus aureus in pigs. Vet Microbiol. 2012;155(2–4):381–8. https://doi.org/10.1016/j.vetmic.2011.09.010 .
doi: 10.1016/j.vetmic.2011.09.010
pubmed: 21963419
Zaatout N, Ayachi A, Kecha M. Staphylococcus aureus persistence properties associated with bovine mastitis and alternative therapeutic modalities. J Appl Microbiol. 2020;129(5):1102–19. https://doi.org/10.1111/jam.14706 .
doi: 10.1111/jam.14706
pubmed: 32416020
Achek R, El-Adawy H, Hotzel H, Tomaso H, Ehricht R, Hamdi TM, et al. Short communication: diversity of staphylococci isolated from sheep mastitis in northern algeria. J Dairy Sci. 2020;103(1):890–7. https://doi.org/10.3168/jds.2019-16583 .
doi: 10.3168/jds.2019-16583
pubmed: 31733855
Mørk T, Kvitle B, Mathisen T, Jørgensen HJ. Bacteriological and molecular investigations of Staphylococcus aureus in dairy goats. Vet Microbiol. 2010;141(1–2):134–41. https://doi.org/10.1016/j.vetmic.2009.08.019 .
Penadés M, Viana D, García-Quirós A, Muñoz-Silvestre A, Moreno-Grua E, Pérez-Fuentes S, et al. Differences in virulence between the two more prevalent Staphylococcus aureus clonal complexes in rabbitries (CC121 and CC96) using an experimental model of mammary gland infection. Vet Res. 2020;51:11. https://doi.org/10.1186/s13567-020-0740-1 .
doi: 10.1186/s13567-020-0740-1
pubmed: 32054530
pmcid: 7020377
Cefai C, Ashurst S, Owens C. Human carriage of methicillin-resistant Staphylococcus aureus linked with pet dog. Lancet. 1994;344(8921):539–40. https://doi.org/10.1016/s0140-6736(94)91926-7 .
doi: 10.1016/s0140-6736(94)91926-7
pubmed: 7914628
Uhlemann AC, McAdam PR, Sullivan SB, Knox JR, Khiabanian H, Rabadan R, et al. Evolutionary dynamics of pandemic methicillin-sensitive Staphylococcus aureus ST398 and Its international spread via routes of human migration. mBio. 2017;8(1):e01375-16. https://doi.org/10.1128/mBio.01375-16 .
Hansen JE, Stegger M, Pedersen K, Sieber RN, Larsen J, Larsen G, et al. Spread of LA-MRSA CC398 in danish mink (Neovison vison) and mink farm workers. Vet Microbiol. 2020;245:108705. https://doi.org/10.1016/j.vetmic.2020.108705 .
doi: 10.1016/j.vetmic.2020.108705
pubmed: 32456821
Alkuraythi DM, Alkhulaifi MM, Binjomah AZ, Alarwi M, Aldakhil HM, Mujallad MI, et al. Clonal flux and spread of Staphylococcus aureus isolated from meat and Its genetic relatedness to Staphylococcus aureus isolated from patients in Saudi Arabia. Microorganisms. 2023;11(12):2926. https://doi.org/10.3390/microorganisms11122926 .
Zhu Z, Wu S, Chen X, Tan W, Zou G, Huang Q, et al. Heterogeneity and transmission of food safety-related enterotoxigenic Staphylococcus aureus in pig abattoirs in Hubei, China. Microbiol Spectr. 2023;11(5):e0191323. https://doi.org/10.1128/spectrum.01913-23 .
doi: 10.1128/spectrum.01913-23
pubmed: 37772855
Yan J, Yang R, Yu S, Zhao W. The application of the lytic domain of endolysin from Staphylococcus aureus bacteriophage in milk. J Dairy Sci. 2021;104(3):2641–53. https://doi.org/10.3168/jds.2020-19456 .
doi: 10.3168/jds.2020-19456
pubmed: 33358804
Titouche Y, Akkou M, Houali K, Auvray F, Hennekinne JA. Role of milk and milk products in the spread of methicillin-resistant Staphylococcus aureus in the dairy production chain. J Food Sci. 2022;87(9):3699–723. https://doi.org/10.1111/1750-3841.16259 .
doi: 10.1111/1750-3841.16259
pubmed: 35894258
Avberšek J, Golob M, Papić B, Dermota U, Grmek Košnik I, Kušar D, et al. Livestock-associated methicillin-resistant Staphylococcus aureus: establishing links between animals and humans on livestock holdings. Transbound Emerg Dis. 2021;68(2):789–801. https://doi.org/10.1111/tbed.13745 .
doi: 10.1111/tbed.13745
pubmed: 32687685
Xu X, Zhou W, Xie C, Zhu Y, Tang W, Zhou X, et al. Airborne bacterial communities in the poultry farm and their relevance with environmental factors and antibiotic resistance genes. Sci Total Environ. 2022;846:157420. https://doi.org/10.1016/j.scitotenv.2022.157420 .
doi: 10.1016/j.scitotenv.2022.157420
pubmed: 35850323
Wang Y, Zhang P, Wu J, Chen S, Jin Y, Long J, et al. Transmission of livestock-associated methicillin-resistant Staphylococcus aureus between animals, environment, and humans in the farm. Environ Sci Pollut Res Int. 2023;30(37):86521–39. https://doi.org/10.1007/s11356-023-28532-7 .
doi: 10.1007/s11356-023-28532-7
pubmed: 37418185
Barberio A, Mazzolini E, Dall’Ava B, Rosa G, Brunetta R, Zandonà L, et al. A longitudinal case study on dissemination of ST398 methicillin-resistant Staphylococcus aureus within a dairy cow herd. Foodborne Pathog Dis. 2019;16(11):761–8. https://doi.org/10.1089/fpd.2019.2622 .
doi: 10.1089/fpd.2019.2622
pubmed: 31225744
Stanton IC, Murray AK, Zhang L, Snape J, Gaze WH. Evolution of antibiotic resistance at low antibiotic concentrations including selection below the minimal selective concentration. Commun Biol. 2020;3:467. https://doi.org/10.1038/s42003-020-01176-w .
doi: 10.1038/s42003-020-01176-w
pubmed: 32884065
pmcid: 7471295
Turner NA, Sharma-Kuinkel BK, Maskarinec SA, Eichenberger EM, Shah PP, Carugati M, et al. Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nat Rev Microbiol. 2019;17(4):203–18. https://doi.org/10.1038/s41579-018-0147-4 .
doi: 10.1038/s41579-018-0147-4
pubmed: 30737488
pmcid: 6939889
Mlynarczyk-Bonikowska B, Kowalewski C, Krolak-Ulinska A, Marusza W. Molecular mechanisms of drug resistance in Staphylococcus aureus. Int J Mol Sci. 2022;23(15):8088. https://doi.org/10.3390/ijms23158088 .
He Y, Yuan Q, Mathieu J, Stadler L, Senehi N, Sun R, et al. Antibiotic resistance genes from livestock waste: occurrence, dissemination, and treatment. NPJ Clean Water. 2020;3:4. https://doi.org/10.1038/s41545-020-0051-0 .
doi: 10.1038/s41545-020-0051-0
Demontier E, Dubé-Duquette A, Brouillette E, Larose A, Ster C, Lucier JF, et al. Relative virulence of Staphylococcus aureus bovine mastitis strains representing the main Canadian spa types and clonal complexes as determined using in vitro and in vivo mastitis models. J Dairy Sci. 2021;104(11):11904–21. https://doi.org/10.3168/jds.2020-19904 .
doi: 10.3168/jds.2020-19904
pubmed: 34454755
de Almeida LM, de Almeida MZ, de Mendonça CL, Mamizuka EM. Comparative analysis of agr groups and virulence genes among subclinical and clinical mastitis Staphylococcus aureus isolates from sheep flocks of the Northeast of Brazil. Braz J Microbiol. 2013;44(2):493–8. https://doi.org/10.1590/s1517-83822013000200026 .
doi: 10.1590/s1517-83822013000200026
pubmed: 24294245
pmcid: 3833151
Bergonier D, de Crémoux R, Rupp R, Lagriffoul G, Berthelot X. Mastitis of dairy small ruminants. Vet Res. 2003;34(5):689–716. https://doi.org/10.1051/vetres:2003030 .
doi: 10.1051/vetres:2003030
pubmed: 14556701
Vasiu I, Wochnik M, Dąbrowski R. Mammary gland inflammation in rabbits does (Oryctolagus cuniculus): a systematic review. Reprod Domest Anim. 2023;58(11):1512–24. https://doi.org/10.1111/rda.14466 .
doi: 10.1111/rda.14466
pubmed: 37650360
Weimer SL, Wideman RF, Scanes CG, Mauromoustakos A, Christensen KD, Vizzier-Thaxton Y. Impact of experimentally induced bacterial chondronecrosis with osteomyelitis (BCO) lameness on health, stress, and leg health parameters in broilers. Poult Sci. 2021;100(11):101457. https://doi.org/10.1016/j.psj.2021.101457 .
doi: 10.1016/j.psj.2021.101457
pubmed: 34607149
pmcid: 8496169
Pati BA, Kurata WE, Horseman TS, Pierce LM. Antibiofilm activity of chitosan/epsilon-poly-L-lysine hydrogels in a porcine ex vivo skin wound polymicrobial biofilm model. Wound Repair Regen. 2021;29(2):316–26. https://doi.org/10.1111/wrr.12890 .
doi: 10.1111/wrr.12890
pubmed: 33480137
Sharma D, Misba L, Khan AU. Antibiotics versus biofilm: an emerging battleground in microbial communities. Antimicrob Resist Infect Control. 2019;8:76. https://doi.org/10.1186/s13756-019-0533-3 .
doi: 10.1186/s13756-019-0533-3
pubmed: 31131107
pmcid: 6524306
Qu Y, Zhao H, Nobrega DB, Cobo ER, Han B, Zhao Z, et al. Molecular epidemiology and distribution of antimicrobial resistance genes of Staphylococcus species isolated from Chinese dairy cows with clinical mastitis. J Dairy Sci. 2019;102(2):1571–83. https://doi.org/10.3168/jds.2018-15136 .
doi: 10.3168/jds.2018-15136
pubmed: 30591326
Jonas OlgaB, Irwin A, Berthe FCJ, Le Gall FG, Marquez PV. Drug-resistant infections: a threat to our economic future (Vol. 2): final report (English). HNP/Agriculture Global Antimicrobial Resistance Initiative Washington, D.C.: World Bank Group. 2007. http://documents.worldbank.org/curated/en/323311493396993758/final-report .
Vergara A, Normanno G, Di Ciccio P, Pedonese F, Nuvoloni R, Parisi A, et al. Biofilm formation and its relationship with the molecular characteristics of food-related methicillin-resistant Staphylococcus aureus (MRSA). J Food Sci. 2017;82(10):2364–70. https://doi.org/10.1111/1750-3841.13846 .
doi: 10.1111/1750-3841.13846
pubmed: 28892140
Vázquez-Sánchez D, Galvão JA, Oetterer M. Contamination sources, biofilm-forming ability and biocide resistance of Staphylococcus aureus in tilapia-processing facilities. Food Sci Technol Int. 2018;24(3):209–22. https://doi.org/10.1177/1082013217742753 .
doi: 10.1177/1082013217742753
pubmed: 29169268
Lee GY, Lee SI, Kim SD, Park JH, Kim GB, Yang SJ. Clonal distribution and antimicrobial resistance of methicillin-susceptible and -resistant Staphylococcus aureus strains isolated from broiler farms, slaughterhouses, and retail chicken meat. Poult Sci. 2022;101(10):102070. https://doi.org/10.1016/j.psj.2022.102070 .
doi: 10.1016/j.psj.2022.102070
pubmed: 36041389
pmcid: 9449669
Qian C, Castañeda-Gulla K, Sattlegger E, Mutukumira AN. Enterotoxigenicity and genetic relatedness of Staphylococcus aureus in a commercial poultry plant and poultry farm. Int J Food Microbiol. 2022;363:109454. https://doi.org/10.1016/j.ijfoodmicro.2021.109454 .
doi: 10.1016/j.ijfoodmicro.2021.109454
pubmed: 34756454
Watkins KE, Unnikrishnan M. Evasion of host defenses by intracellular Staphylococcus aureus. Adv Appl Microbiol. 2020;112:105–41. https://doi.org/10.1016/bs.aambs.2020.05.001 .
doi: 10.1016/bs.aambs.2020.05.001
pubmed: 32762866
Stelzner K, Winkler A-C, Liang C, Boyny A, Ade CP, Dandekar T, et al. Intracellular Staphylococcus aureus perturbs the host cell Ca
Schönborn S, Krömker V. Detection of the biofilm component polysaccharide intercellular adhesin in Staphylococcus aureus infected cow udders. Vet Microbiol. 2016;196:126–8. https://doi.org/10.1016/j.vetmic.2016.10.023 .
doi: 10.1016/j.vetmic.2016.10.023
pubmed: 27939148
Foster TJ. The MSCRAMM family of cell-wall-anchored surface proteins of gram-positive cocci. Trends Microbiol. 2019;27(11):927–41. https://doi.org/10.1016/j.tim.2019.06.007 .
doi: 10.1016/j.tim.2019.06.007
pubmed: 31375310
Campos B, Pickering AC, Rocha LS, Aguilar AP, Fabres-Klein MH, de Oliveira Mendes TA, et al. Diversity and pathogenesis of Staphylococcus aureus from bovine mastitis: current understanding and future perspectives. BMC Vet Res. 2022;18:115. https://doi.org/10.1186/s12917-022-03197-5 .
doi: 10.1186/s12917-022-03197-5
pubmed: 35331225
pmcid: 8944054
Leuenberger A, Sartori C, Boss R, Resch G, Oechslin F, Steiner A, et al. Genotypes of Staphylococcus aureus: On-farm epidemiology and the consequences for prevention of intramammary infections. J Dairy Sci. 2019;102(4):3295–309. https://doi.org/10.3168/jds.2018-15181 .
doi: 10.3168/jds.2018-15181
pubmed: 30738682
Schilcher K, Horswill AR. Staphylococcal biofilm development: structure, regulation, and treatment strategies. Microbiol Mol Biol Rev. 2020;84(3):e00026-19. https://doi.org/10.1128/MMBR.00026-19 .
Peng Q, Tang X, Dong W, Sun N, Yuan W. A review of biofilm formation of Staphylococcus aureus and its regulation mechanism. Antibiotics. 2022;12(1):12. https://doi.org/10.3390/antibiotics12010012 .
doi: 10.3390/antibiotics12010012
pubmed: 36671212
pmcid: 9854888
Foster TJ. Surface proteins of Staphylococcus aureus. Microbiol Spectr. 2019;7(4). https://doi.org/10.1128/microbiolspec.GPP3-0046-2018 .
Thewes N, Loskill P, Jung P, Peisker H, Bischoff M, Herrmann M, et al. Hydrophobic interaction governs unspecific adhesion of Staphylococci: a single cell force spectroscopy study. Beilstein J Nanotechnol. 2014;5(1):1501–12. https://doi.org/10.3762/bjnano.5.163 .
doi: 10.3762/bjnano.5.163
pubmed: 25247133
pmcid: 4168904
Sinsinwar S, Jayaraman A, Mahapatra SK, Vellingiri V. Anti-virulence properties of catechin-in-cyclodextrin-in-phospholipid liposome through down-regulation of gene expression in MRSA strains. Microb Pathog. 2022;167:105585. https://doi.org/10.1016/j.micpath.2022.105585 .
doi: 10.1016/j.micpath.2022.105585
pubmed: 35569694
Okshevsky M, Meyer RL. The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Crit Rev Microbiol. 2015;41(3):341–52. https://doi.org/10.3109/1040841X.2013.841639 .
doi: 10.3109/1040841X.2013.841639
pubmed: 24303798
Moormeier DE, Bayles KW. Staphylococcus aureus biofilm: a complex developmental organism. Mol Microbiol. 2017;104(3):365–76. https://doi.org/10.1111/mmi.13634 .
Tomlinson KL, Lung TWF, Dach F, Annavajhala MK, Gabryszewski SJ, Groves RA, et al. Staphylococcus aureus induces an itaconate-dominated immunometabolic response that drives biofilm formation. Nat Commun. 2021;12:1399. https://doi.org/10.1038/s41467-021-21718-y .
Thammavongsa V, Missiakas DM, Schneewind O. Staphylococcus aureus degrades neutrophil extracellular traps to promote immune cell death. Science. 2013;342(6160):863–6. https://doi.org/10.1126/science.1242255 .
doi: 10.1126/science.1242255
pubmed: 24233725
pmcid: 4026193
Taglialegna A, Navarro S, Ventura S, Garnett JA, Matthews S, Penades JR, et al. Staphylococcal bap proteins build amyloid scaffold biofilm matrices in response to environmental signals. PLoS Pathog. 2016;12(6):e1005711. https://doi.org/10.1371/journal.ppat.1005711 .
doi: 10.1371/journal.ppat.1005711
pubmed: 27327765
pmcid: 4915627
Paharik AE, Kotasinska M, Both A, Hoang TN, Buttner H, Roy P, et al. The metalloprotease SepA governs processing of accumulation-associated protein and shapes intercellular adhesive surface properties in Staphylococcus epidermidis. Mol Microbiol. 2017;103(5):860–74. https://doi.org/10.1111/mmi.13594 .
doi: 10.1111/mmi.13594
pubmed: 27997732
pmcid: 5480372
Speziale P, Pietrocola G. The multivalent role of fibronectin-binding proteins A and B (FnBPA and FnBPB) of Staphylococcus aureus in host infections. Front Microbiol. 2020;11:2054. https://doi.org/10.3389/fmicb.2020.02054 .
doi: 10.3389/fmicb.2020.02054
pubmed: 32983039
pmcid: 7480013
Wang L, Wang H, Zhang H, Wu H. Formation of a biofilm matrix network shapes polymicrobial interactions. ISME J. 2023;17(3):467–77. https://doi.org/10.1038/s41396-023-01362-8 .
doi: 10.1038/s41396-023-01362-8
pubmed: 36639539
pmcid: 9938193
Deng W, Lei Y, Tang X, Li D, Liang J, Luo J, et al. DNase inhibits early biofilm formation in Pseudomonas aeruginosa-or Staphylococcus aureus-induced empyema models. Front Cell Infect Microbiol. 2022;12:917038. https://doi.org/10.3389/fcimb.2022.917038 .
Ma Y, Deng Y, Hua H, Khoo BL, Chua SL. Distinct bacterial population dynamics and disease dissemination after biofilm dispersal and disassembly. ISME J. 2023;17(8):1290–302. https://doi.org/10.1038/s41396-023-01446-5 .
doi: 10.1038/s41396-023-01446-5
pubmed: 37270584
Grando K, Nicastro LK, Tursi SA, De Anda J, Lee EY, Wong GC, et al. Phenol-soluble modulins from Staphylococcus aureus biofilms form complexes with DNA to drive autoimmunity. Front Cell Infect Microbiol. 2022;12:517. https://doi.org/10.3389/fcimb.2022.884065 .
doi: 10.3389/fcimb.2022.884065
Deepika G, Subbarayadu S, Chaudhary A, Sarma P. Dibenzyl (benzo [d] thiazol-2-yl (hydroxy) methyl) phosphonate (DBTMP) showing anti-S. aureus and anti-biofilm properties by elevating activities of serine protease (SspA) and cysteine protease staphopain B (SspB). Arch Microbiol. 2022;204(7):397. https://doi.org/10.1007/s00203-022-02974-y .
doi: 10.1007/s00203-022-02974-y
pubmed: 35708833
Wang Y, Bian Z, Wang Y. Biofilm formation and inhibition mediated by bacterial quorum sensing. Appl Microbiol Biotechnol. 2022;106(19–20):6365–81. https://doi.org/10.1007/s00253-022-12150-3 .
doi: 10.1007/s00253-022-12150-3
pubmed: 36089638
Paharik AE, Horswill AR. The staphylococcal biofilm: adhesins, regulation, and host response. Microbiol Spectr. 2016;4(2):529–66. https://doi.org/10.1128/microbiolspec.VMBF-0022-2015 .
Hespanhol JT, Sanchez-Limache DE, Nicastro GG, Mead L, Llontop EE, Chagas-Santos G, et al. Antibacterial T6SS effectors with a VRR-Nuc domain are structure-specific nucleases. Elife. 2022;11:e82437. https://doi.org/10.7554/eLife.82437 .
doi: 10.7554/eLife.82437
pubmed: 36226828
pmcid: 9635880
Tan P, Wu C, Tang Q, Wang T, Zhou C, Ding Y, et al. pH-triggered size-transformable and bioactivity-switchable self-assembling chimeric peptide nanoassemblies for combating drug-resistant bacteria and biofilms. Adv Mater. 2023;35:2210766. https://doi.org/10.1002/adma.202210766 .
Xu S, Tan P, Tang Q, Wang T, Ding Y, Fu H, et al. Enhancing the stability of antimicrobial peptides: From design strategies to biomedical applications. Chem Eng J. 2023:145923. https://doi.org/10.1016/j.cej.2023.145923 .
Zhang Y, Tan P, Zhao Y, Ma X. Enterotoxigenic Escherichia coli: Intestinal pathogenesis mechanisms and colonization resistance by gut microbiota. Gut Microbes. 2022;14(1):2055943. https://doi.org/10.1080/19490976.2022.2055943 .
doi: 10.1080/19490976.2022.2055943
pubmed: 35358002
pmcid: 8973357
Tang Q, Tan P, Dai Z, Wang T, Xu S, Ding Y, et al. Hydrophobic modification improves the delivery of cell-penetrating peptides to eliminate intracellular pathogens in animals. Acta Biomater. 2023;157:210–24. https://doi.org/10.1016/j.actbio.2022.11.055 .
doi: 10.1016/j.actbio.2022.11.055
pubmed: 36503077
Tan P, Sun Z, Tang Q, Xu S, Wang T, Ding Y, et al. Manipulation of hydrophobic motifs and optimization of sequence patterns to design high stability peptides against piglet bacterial infections. Nano Today. 2023;49:101793. https://doi.org/10.1016/j.nantod.2023.101793 .
doi: 10.1016/j.nantod.2023.101793
Xu S, Tan P, Tang Q, Wang T, Ding Y, Zhou C, et al. Design of high-selectivity co-assembled peptide nanofibers against bacterial infection in piglets. ACS Appl Mater Interfaces. 2023. https://doi.org/10.1021/acsami.3c03758 .
doi: 10.1021/acsami.3c03758
pubmed: 38157482
pmcid: 10614196
Libardo MDJ, Bahar AA, Ma BY, Fu RQ, McCormick LE, Zhao J, et al. Nuclease activity gives an edge to host-defense peptide piscidin 3 over piscidin 1, rendering it more effective against persisters and biofilms. Febs J. 2017;284(21):3662–83. https://doi.org/10.1111/febs.14262 .
doi: 10.1111/febs.14262
pubmed: 28892294
pmcid: 6361529
Popitool K, Wataradee S, Wichai T, Noitang S, Ajariyakhajorn K, Charoenrat T, et al. Potential of Pm11 antimicrobial peptide against bovine mastitis pathogens. Am J Vet Res. 2023;84(1). https://doi.org/10.2460/ajvr.22.06.0096 .
Shah P, Shrivastava S, Gogoi P, Saxena S, Srivastava S, Singh RJ, et al. Wasp venom peptide (Polybia MP-1) shows antimicrobial activity against multi drug resistant bacteria isolated from mastitic cow milk. Int J Pept Res Ther. 2022;28:44. https://doi.org/10.1007/s10989-021-10355-0 .
doi: 10.1007/s10989-021-10355-0
Gogoi P, Shrivastava S, Shah P, Saxena S, Srivastava S, Gaur GK. Linear and branched forms of short antimicrobial peptide-IRK inhibit growth of multi drug resistant Staphylococcus aureus isolates from mastitic cow milk. Int J Pept Res Ther. 2021;27:2149–59. https://doi.org/10.1007/s10989-021-10243-7 .
doi: 10.1007/s10989-021-10243-7
Field D, Considine K, O’Connor PM, Ross RP, Hill C, Cotter PD. Bio-engineered nisin with increased anti-Staphylococcus and selectively reduced anti-Lactococcus activity for treatment of bovine mastitis. Int J Mol Sci. 2021;22(7):3480. https://doi.org/10.3390/ijms22073480 .
doi: 10.3390/ijms22073480
pubmed: 33801752
pmcid: 8036683
Fei F, Wang T, Jiang Y, Chen X, Ma C, Zhou M, et al. A frog-derived antimicrobial peptide as a potential anti-biofilm agent in combating Staphylococcus aureus skin infection. J Cell Mol Med. 2023. https://doi.org/10.1111/jcmm.17785 .
doi: 10.1111/jcmm.17785
pubmed: 37909722
pmcid: 10805501
Jiang M, Yang X, Wu H, Huang Y, Dou J, Zhou C, et al. An active domain HF-18 derived from hagfish intestinal peptide effectively inhibited drug-resistant bacteria in vitro/vivo. Biochem Pharmacol. 2020;172:113746. https://doi.org/10.1016/j.bcp.2019.113746 .
doi: 10.1016/j.bcp.2019.113746
pubmed: 31812678
Gil J, Pastar I, Houghten RA, Padhee S, Higa A, Solis M, et al. Novel cyclic lipopeptides fusaricidin analogs for treating wound infections. Front Microbiol. 2021;12:708904. https://doi.org/10.3389/fmicb.2021.708904 .
doi: 10.3389/fmicb.2021.708904
pubmed: 34367114
pmcid: 8343139
Sangboonruang S, Semakul N, Obeid MA, Ruano M, Kitidee K, Anukool U, et al. Potentiality of melittin-loaded niosomal vesicles against vancomycin-intermediate Staphylococcus aureus and Staphylococcal skin infection. Int J Nanomedicine. 2021:7639–61. https://doi.org/10.2147/IJN.S325901 .
Kim H-S, Jang Y, Ham S-Y, Park J-H, Kang H-J, Yun ET, et al. Effect of broad-spectrum biofilm inhibitor raffinose, a plant galactoside, on the inhibition of co-culture biofilm on the microfiltration membrane. J Hazard Mater. 2021;402:123501. https://doi.org/10.1016/j.jhazmat.2020.123501 .
doi: 10.1016/j.jhazmat.2020.123501
pubmed: 32712354
Zhan K, Yang T, Feng B, Zhu X, Chen Y, Huo Y, et al. The protective roles of tea tree oil extracts in bovine mammary epithelial cells and polymorphonuclear leukocytes. J Anim Sci Biotechnol. 2020;11:62. https://doi.org/10.1186/s40104-020-00468-9 .
Forno-Bell N, Bucarey SA, García D, Iragüen D, Chacón O, San Martín B. Antimicrobial effects caused by aloe barbadensis miller on bacteria associated with mastitis in dairy cattle. Nat Prod Commun. 2019;14(12):1934578X19896670. https://doi.org/10.1177/1934578X19896670 .
doi: 10.1177/1934578X19896670
Abd El-Hamid MI, El-Tarabili RM, Bahnass MM, Alshahrani MA, Saif A, Alwutayd KM, et al. Partnering essential oils with antibiotics: proven therapies against bovine Staphylococcus aureus mastitis. Front Cell Infect Microbiol. 2023;13. https://doi.org/10.3389/fcimb.2023.1265027 .
Abreu AC, Saavedra MJ, Simões LC, Simões M. Combinatorial approaches with selected phytochemicals to increase antibiotic efficacy against Staphylococcus aureus biofilms. Biofouling. 2016;32(9):1103–14. https://doi.org/10.1080/08927014.2016.1232402 .
doi: 10.1080/08927014.2016.1232402
pubmed: 27643487
Srichok J, Yingbun N, Kowawisetsut T, Kornmatitsuk S, Suttisansanee U, Temviriyanukul P, et al. Synergistic antibacterial and anti-inflammatory activities of Ocimum tenuiflorum ethanolic extract against major bacterial mastitis pathogens. Antibiotics. 2022;11(4):510. https://doi.org/10.3390/antibiotics11040510 .
Nwabueze A, Ekelemu J, Owe O. Response of Clarias gariepinus to Allium sativum-based diet on growth performance and Staphylococcus aureus challenge infection. J Appl Sci Environ Manage. 2020;24(5):755–9. https://doi.org/10.4314/jasem.v24i5.4 .
Hill EK, Li J. Current and future prospects for nanotechnology in animal production. J Anim Sci Biotechnol. 2017;8:26. https://doi.org/10.1186/s40104-017-0157-5 .
Mohd Yusof H, Mohamad R, Zaidan UH, Abdul Rahman NA. Microbial synthesis of zinc oxide nanoparticles and their potential application as an antimicrobial agent and a feed supplement in animal industry: a review. J Anim Sci Biotechnol. 2019;10:57. https://doi.org/10.1186/s40104-019-0368-z .
Tan P, Fu H, Ma X. Design, optimization, and nanotechnology of antimicrobial peptides: From exploration to applications. Nano Today. 2021;39:101229. https://doi.org/10.1016/j.nantod.2021.101229 .
doi: 10.1016/j.nantod.2021.101229
Jagielski T, Bakuła Z, Pleń M, Kamiński M, Nowakowska J, Bielecki J, et al. The activity of silver nanoparticles against microalgae of the Prototheca genus. Nanomedicine. 2018;13(9):1025–36. https://doi.org/10.2217/nnm-2017-0370 .
doi: 10.2217/nnm-2017-0370
pubmed: 29790400
Kalińska A, Jaworski S, Wierzbicki M, Gołębiewski M. Silver and copper nanoparticles—an alternative in future mastitis treatment and prevention? Int J Mol Sci. 2019;20(7):1672. https://doi.org/10.3390/ijms20071672 .
doi: 10.3390/ijms20071672
pubmed: 30987188
pmcid: 6480535
Ul-Hamid A, Dafalla H, Hakeem AS, Haider A, Ikram M. In-vitro catalytic and antibacterial potential of green synthesized CuO nanoparticles against prevalent multiple drug resistant bovine mastitogen Staphylococcus aureus. Int J Mol Sci. 2022;23(4):2335. https://doi.org/10.3390/ijms23042335 .
doi: 10.3390/ijms23042335
pubmed: 35216450
pmcid: 8878101
Taifa S, Muhee A, Bhat RA, Nabi SU, Roy A, Rather GA, et al. Evaluation of therapeutic efficacy of copper nanoparticles in Staphylococcus aureus-induced rat mastitis model. J Nanomater. 2022;2022. https://doi.org/10.1155/2022/7124114 .
Mahmoud UT, Darwish MH, Ali FAZ, Amen OA, Mahmoud MA, Ahmed OB, et al. Zinc oxide nanoparticles prevent multidrug resistant Staphylococcus-induced footpad dermatitis in broilers. Avian Pathol. 2021;50(3):214–26. https://doi.org/10.1080/03079457.2021.1875123 .
doi: 10.1080/03079457.2021.1875123
Younus N, Zuberi A, Mahmoood T, Akram W, Ahmad M. Comparative effects of dietary micro-and nano-scale chitosan on the growth performance, non-specific immunity, and resistance of silver carp Hypophthalmichthys molitrix against Staphylococcus aureus infection. Aquacult Int. 2020;28:2363–78. https://doi.org/10.1007/s10499-020-00595-0 .
doi: 10.1007/s10499-020-00595-0
Elsayed MM, Elgohary FA, Zakaria AI, Elkenany RM, El-Khateeb AY. Novel eradication methods for Staphylococcus aureus biofilm in poultry farms and abattoirs using disinfectants loaded onto silver and copper nanoparticles. Environ Sci Pollut Res. 2020;27:30716–28. https://doi.org/10.1007/s11356-020-09340-9 .
doi: 10.1007/s11356-020-09340-9
Tan P, Tang Q, Xu S, Zhang Y, Fu H, Ma X. Designing self-assembling chimeric peptide nanoparticles with high stability for combating piglet bacterial infections. Adv Sci. 2022;9(14):e2105955. https://doi.org/10.1002/advs.202105955 .
Gordillo Altamirano FL, Barr JJ. Phage therapy in the postantibiotic era. Clin Microbiol Rev. 2019;32(2):00066–18. https://doi.org/10.1128/CMR.00066-18 .
doi: 10.1128/CMR.00066-18
Hansen MF, Svenningsen SL, Røder HL, Middelboe M, Burmølle M. Big impact of the tiny: Bacteriophage-bacteria interactions in biofilms. Trends Microbiol. 2019;27(9):739–52. https://doi.org/10.1016/j.tim.2019.04.006 .
Gutierrez D, Vandenheuvel D, Martinez B, Rodriguez A, Lavigne R, Garcia P. Two phages, phiIPLA-RODI and phiIPLA-C1C, lyse mono- and dual-species staphylococcal biofilms. Appl Environ Microb. 2015;81(10):3336–48. https://doi.org/10.1128/Aem.03560-14 .
Alves DR, Gaudion A, Bean JE, Esteban PP, Arnot TC, Harper DR, et al. Combined use of bacteriophage K and a novel bacteriophage to reduce Staphylococcus aureus biofilm formation. Appl Environ Microb. 2014;80(21):6694–703. https://doi.org/10.1128/Aem.01789-14 .
Tuomala H, Verkola M, Meller A, Van der Auwera J, Patpatia S, Järvinen A, et al. Phage treatment trial to eradicate LA-MRSA from healthy carrier pigs. Viruses. 2021;13(10):1888. https://doi.org/10.3390/v13101888 .
doi: 10.3390/v13101888
pubmed: 34696318
pmcid: 8539482
Drilling A, Morales S, Boase S, Jervis-Bardy J, James C, Jardeleza C, et al. Safety and efficacy of topical bacteriophage and ethylenediaminetetraacetic acid treatment of Staphylococcus aureus infection in a sheep model of sinusitis. Int Forum Allergy Rhinol. 2014;4(3):176–86. https://doi.org/10.1002/alr.21270 .
doi: 10.1002/alr.21270
pubmed: 24449635
Drilling AJ, Ooi ML, Miljkovic D, James C, Speck P, Vreugde S, et al. Long-term safety of topical bacteriophage application to the frontal sinus region. Front Cell Infect Microbiol. 2017;7:49. https://doi.org/10.3389/fcimb.2017.00049 .
doi: 10.3389/fcimb.2017.00049
pubmed: 28286740
pmcid: 5323412
Srujana A, Sonalika J, Akhila D, Juliet M, Sheela P. Isolation of phages and study of their in vitro efficacy on Staphylococcus aureus isolates originating from bovine subclinical mastitis. Indian J Anim Res. 2022;56:754–8. https://doi.org/10.18805/IJAR.B-4331 .
doi: 10.18805/IJAR.B-4331
Brouillette E, Millette G, Chamberland S, Roy JP, Ster C, Kiros T, et al. Effective treatment of Staphylococcus aureus intramammary infection in a murine model using the bacteriophage cocktail StaphLyse™. viruses. 2023;15(4):887. https://doi.org/10.3390/v15040887 .
doi: 10.3390/v15040887
pubmed: 37112867
pmcid: 10145274
Suresh MK, Biswas R, Biswas L. An update on recent developments in the prevention and treatment of Staphylococcus aureus biofilms. Int J Med Microbiol. 2019;309(1):1–12. https://doi.org/10.1016/j.ijmm.2018.11.002 .
doi: 10.1016/j.ijmm.2018.11.002
pubmed: 30503373
Nair N, Vinod V, Suresh MK, Vijayrajratnam S, Biswas L, Peethambaran R, et al. Amidase, a cell wall hydrolase, elicits protective immunity against Staphylococcus aureus and S. epidermidis. Int J Biol Macromol. 2015;77:314–21. https://doi.org/10.1016/j.ijbiomac.2015.03.047 .
Estelles A, Woischnig AK, Liu KY, Stephenson R, Lomongsod E, Nguyen D, et al. A high-affinity native human antibody disrupts biofilm from Staphylococcus aureus bacteria and potentiates antibiotic efficacy in a mouse implant infection model. Antimicrob Agents Ch. 2016;60(4):2292–301. https://doi.org/10.1128/Aac.02588-15 .
doi: 10.1128/Aac.02588-15
Lam H, Kesselly A, Stegalkina S, Kleanthous H, Yethon JA. Antibodies to PhnD inhibit Staphylococcal biofilms. Infect Immun. 2014;82(9):3764–74. https://doi.org/10.1128/Iai.02168-14 .
doi: 10.1128/Iai.02168-14
pubmed: 24958708
pmcid: 4187816
Wang M, Wang T, Guan Y, Wang F, Zhu J. The preparation and therapeutic roles of scFv-Fc antibody against Staphylococcus aureus infection to control bovine mastitis. Appl Microbiol Biotechnol. 2019;103(4):1703–12. https://doi.org/10.1007/s00253-018-9548-6 .
doi: 10.1007/s00253-018-9548-6
pubmed: 30607490