Abstract
Infections due to methicillin-resistant Staphylococcus aureus (MRSA) are a growing concern for public health resulting in increase in morbidity, length of hospital stay, and cost of treatment. MRSA nasal swab screening may give clinicians additional information for decision of empiric antimicrobial agents. While increasing antibiotic resistance leads to new treatment approaches, bacteriophages are one of the most promising methods for these alternatives. It was aimed to determine the effectiveness of bacteriophages against MRSA isolates. Nasal swab samples were collected from outpatients without any evidence of infection who applied to Hatay, Mersin and Gaziantep family and immigration health centers. A series (35) were isolated from Turkish patients, and G series (64) were isolated from Syrian immigrants. Methicillin resistance was determined phenotypically and genotypically. Also, antibiotic susceptibilities of all isolates were determined against erythromycin, clindamycin, gentamicin, linezolid, rifampicin, and mupirocin. The total antimicrobial resistance rates of isolates were found to be 11%, 28%, 8%, 5%, 16%, 19%, and 29% respectively. The high susceptibility rate against ciprofloxacin (88.8%) was remarkable. The overall susceptibility of MRSA strains to ENKO, INTESTI, PYO, SES, and staphylococcal bacteriophages was 67.7%, 55.5%, 53.5%, 61.6% and 44.4%, respectively. The antibiotic susceptibility rates (except erythromycin) and efficacy of bacteriophages were higher in group A. Considering that high efficacy rates were not achieved in the study and the sensitivity rates of Turkish isolates to all phages were found to be higher than those of Syrian isolates, searching for phages in the geographic regions where the pathogen is common may be helpful to obtain suitable phages for treatment.
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References
Abedon ST, Garcia P, Mullany P, Aminov R (2017) Editorial: phage therapy: past, present and future. Front Microbiol 8:981. https://doi.org/10.3389/fmicb.2017.00981
Alvarez A, Fernandez L, Iglesias B, Rodriguez J, Rodriguez A, Garcia P (2019) Phage therapy: unexpected drawbacks to reach hospitals. Future Virol 14(12):779–782. https://doi.org/10.2217/fvl-2019-0154
Clokie MRJ, Millard AD, Letarov AV, Heaphy S (2011) Phages in nature. Bacteriophage 1:31–45. https://doi.org/10.4161/bact.1.1.14942
Dvorackova M, Ruzicka F, Benesik M, Pantucek R, Dvorakova-Heroldova M (2019) Antimicrobial effect of commercial phage preparation Stafal (R) on biofilm and planktonic forms of methicillin-resistant Staphylococcus aureus. Folia Microbiol 64(1):121–126. https://doi.org/10.1007/s12223-018-0622-3
EUCAST (2021) EUCAST disk diffusion method Version 9.0 January 2021. https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Disk_test_documents/2021_manuals/Manual_v_9.0_EUCAST_Disk_Test_2021.pdf. Accessed 1 July 2021
Goetghebeur M, Landry PA, Han D, Vicente C (2007) Methicillin-resistant Staphylococcus aureus: a public health issue with economic consequences. Can J Infect Dis Med 18(1):27–34. https://doi.org/10.1155/2007/253947
Jennes S, Merabishvili M, Soentjens P, Pang KW, Rose T, Keersebilck E, Soete O, Francois PM, Teodorescu S, Verween G, Verbeken G, De Vos D, Pirnay JP (2017) Use of bacteriophages in the treatment of colistin-only-sensitive Pseudomonas aeruginosa septicaemia in a patient with acute kidney injury-a case report. Crit Care. https://doi.org/10.1186/s13054-017-1709-y
Kuptsov NS, Kornienko MA, Gorodnichev RB, Danilov DI, Malakhova MV, Parfenova N, Makarenko GI, Shitikov EA, Ilina EN (2020) Efficacy of commercial bacteriophage products against eskape pathogens. Bull RSMU. https://doi.org/10.24075/brsmu.2020.029
Lyon J (2017) Phage therapy’s role in combating antibiotic-resistant pathogens. Jama-J Am Med Assoc 318(18):1746–1748. https://doi.org/10.1001/jama.2017.12938
Nir-Paz R, Gelman D, Khouri A, Sisson BM, Fackler J, Alkalay-Oren S, Khalifa L, Rimon A, Yerushalmy O, Bader R, Amit S, Coppenhagen-Glazer S, Henry M, Quinones J, Malagon F, Biswas B, Moses AE, Merril G, Schooley RT, Brownstein MJ, Weil YA, Hazan R (2019) Successful treatment of antibiotic-resistant, poly-microbial bone infection with bacteriophages and antibiotics combination. Clin Infect Dis 69(11):2015–2018. https://doi.org/10.1093/cid/ciz222
Oliveira DC, de Lencastre H (2002) Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 46(7):2155–2161. https://doi.org/10.1128/Aac.46.7.2155-2161.2002
Ozkan I, Akturk E, Yeshenkulov N, Atmaca S, Rahmanov N, Atabay HI (2016) Lytic activity of various phage cocktails on multidrug-resistant bacteria. Clin Invest Med 39(6):S66–S70
Ross A, Ward S, Hyman P (2016) More is better: Selecting for broad host range bacteriophages. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01352
Stegger M, Andersen PS, Kearns A, Pichon B, Holmes MA, Edwards G, Laurent F, Teale C, Skov R, Larsen AR (2012) Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecA(LGA251). Clin Microbiol Infect 18(4):395–400. https://doi.org/10.1111/j.1469-0691.2011.03715.x
Sulakvelidze A, Alavidze Z, Morris JG (2001) Bacteriophage therapy. Antimicrob Agents Chemother 45(3):649–659. https://doi.org/10.1128/Aac.45.3.649-659.2001
Tkhilaishvili T, Winkler T, Muller M, Perka C, Trampuz A (2020) Bacteriophages as adjuvant to antibiotics for the treatment of periprosthetic joint infection caused by multidrug-resistant Pseudomonas aeruginosa. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.00924-19
Wittebole X, De Roock S, Opal SM (2014) A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 5(1):226–235. https://doi.org/10.4161/viru.25991
Zhang KY, Sparling J, Chow BL, Elsayed S, Hussain Z, Church DL, Gregson DB, Louie T, Conly JM (2004) New quadriplex PCR assay for detection of methicillin and mupirocin resistance and simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol 42(11):4947–4955. https://doi.org/10.1128/Jcm.42.11.4947-4955.2004
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Erol, H.B., Kaskatepe, B., Bakkaloglu, Z. et al. The evaluation of five commercial bacteriophage cocktails against methicillin-resistant Staphylococcus aureus isolated from nasal swab samples. Arch Microbiol 203, 5735–5743 (2021). https://doi.org/10.1007/s00203-021-02564-4
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DOI: https://doi.org/10.1007/s00203-021-02564-4