Iranian Journal of War and Public Health

eISSN (English): 2980-969X
eISSN (Persian): 2008-2630
pISSN (Persian): 2008-2622
JMERC
0.3
Volume 14, Issue 3 (2022)                   Iran J War Public Health 2022, 14(3): 351-357 | Back to browse issues page

Print XML PDF HTML Full-Text (HTML)

History

How to cite this article
Al-Mousawi A, Al-Amara S, Humoud M, Hattab S. Frequency of Inducible Clindamycin Resistance in Staphylococcus haemolyticus Isolated from Surgical Wounds Infections Using D-test and Molecular Methods in Al-Basrah, Iraq. Iran J War Public Health 2022; 14 (3) : 100
URL: http://ijwph.ir/article-1-1041-en.html
Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Rights and permissions
1- Department of Biology, College of Science, University of Basrah, Basrah, Iraq
2- Department of Pathological Analysis, College of Science, University of Basrah, Basrah, Iraq
3- Public Health Department, Basrah Health Directorate, Basrah, Iraq
* Corresponding Author Address: (saad.mahdi@uobasrah.edu.iq)
Abstract   (798 Views)
Aims: S. haemolyticus is generally considered an opportunistic pathogen that is strongly associated with immunocompromised individuals. S. haemolyticus is ranked as a highly antibiotic-resistant pathogen for various types of antibiotics. Current study aimed to investigate the frequency of inducible clindamycin resistance in S. haemolyticus isolated from surgical wounds infections using D-test and molecular methods in Al-Basrah, Iraq.
Materials & Methods: 200 surgical wound swabs were collected from Ports General Hospital in Basrah, Iraq. The coagulase-negative staphylococcal strains were identified using methods like oxidase, catalase, hemolysis, and coagulase tests and confirmed by Vitek®2 system. Methicillin resistance and inducible clindamycin resistance were detected according to disk diffusion method based on CLSI guidelines. Moreover, molecular approaches was performed to confirm methicillin and inducible clindamycin resistance results.
Findings: Out of 200 cases, 75 surgical wound swabs (37.5%) showed positive bacterial cultures. The highest frequency of isolates belonged to Pseudomonas aeruginosa (25.3%), Staphylococcus epidermidis (17.3%), Staphylococcus aureus (14.7%) and Escherichia coli (13.3%), respectively. Out of eight S. haemolyticus isolates, only 5 isolates (62.5%) showed inhibitory resistance criteria for both oxacillin and cefoxitin. Furthermore, 3 S. haemolyticus isolates (37.5%) were erythromycin-resistant and clindamycin sensitive with D-test positive with iMLSB resistance phenotype. While 2 isolates (25.0%) showed cMLSB resistance phenotype and 3 (37.5%) isolates were shown MSB resistance phenotypes. The most frequent resistance genes of S. haemolyticus strains were mecA (62.5%), ermA (62.5%), ermB (50.0%), respectively.
Conclusion: D-test and molecular technique are appropriate for detection of inducible clindamycin resistance in S. haemolyticus strains.
Article number: 100
Keywords:

References
1. Turner NA, Sharma-Kuinkel BK, Maskarinec SA, Eichenberger EM, Shah PP, et al. Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nature Rev Microbiol. 2019;17(4):203-18. [Link] [DOI:10.1038/s41579-018-0147-4]
2. Abdullah-Al-Shoeb M, Huq S, Abul Kalam Azad M, Rahman N. Assessment of antibacterial efficacy of Lugol's iodine compared with commercial hand sanitizers of Bangladesh. J World Poultry Res. 2019;9(5):130-7. [Link] [DOI:10.36380/scil.2019.jlsb21]
3. Brook I. Bacteriology of neonatal omphalitis. J Infect. 1982;5(2):127-31. [Link] [DOI:10.1016/S0163-4453(82)91656-5]
4. Bjorkqvist M, Liljedahl M, Zimmermann J, Schollin J, Soderquist B. Colonization pattern of coagulase-negative staphylococci in preterm neonates and the relation to bacteremia. Eur J Clin Microbiol Infect Dis. 2010;29(9):1085-93. [Link] [DOI:10.1007/s10096-010-0966-3]
5. Cave R, Misra R, Chen J, Wang S, Mkrtchyan HV. Whole genome sequencing revealed new molecular characteristics in multidrug resistant staphylococci recovered from high frequency touched surfaces in London. Sci Rep. 2019;9:9637. [Link] [DOI:10.1038/s41598-019-45886-6]
6. Mehri H, Jahanbakhsh R, Shakeri F, Ardebili A, Behnampour N, Khodabakhshi B, Ghaemi EA. Investigation of glycopeptide susceptibility of coagulase-negative staphylococci (CoNS) from a tertiary care hospital in Gorgan, Northern Iran. Arch Pediatr Infect. 2017;5(1):e37264. [Link] [DOI:10.5812/pedinfect.37264]
7. Czekaj T, Ciszewski M, and Szewczyk EM. Staphylococcus haemolyticus-an emerging threat in the twilight of the antibiotics age. Microbiology 2015;161(11):2061-8. [Link] [DOI:10.1099/mic.0.000178]
8. Eltwisy HO, Abdel-Fattah M, Elsisi AM, Omar MM, Abdelmoteleb AA, El-Mokhtar MA. Pathogenesis of Staphylococcus haemolyticus on primary human skin fibroblast cells. Virulence. 2020;11(1):1142-57. [Link] [DOI:10.1080/21505594.2020.1809962]
9. do Carmo Ferreira N, Schuenck RP, Dos Santos KRN, de Freire Bastos M, Giambiagi-deMarval M. Diversity of plasmids and transmission of high-level mupirocin mupA resistance gene in Staphylococcus haemolyticus. FEMS Immunol Med Microbiol. 2011;61(2):147-52. [Link] [DOI:10.1111/j.1574-695X.2010.00756.x]
10. Schuenck RP, Pereira EM, Iorio NLP, Dos Santos KRN. Multiplex PCR assay to identify methicillin-resistant Staphylococcus haemolyticus. FEMS Immunol Med Microbiol. 2008;52(3):431-5. [Link] [DOI:10.1111/j.1574-695X.2008.00387.x]
11. Ruzauskas M, Siugzdiniene R, Klimiene I, Virgailis M, Mockeliunas R, et al. Prevalence of methicillin-resistant Staphylococcus haemolyticus in companion animals: A cross-sectional study. Ann Clin Microbiol Antimicrob. 2014;13:56. [Link] [DOI:10.1186/s12941-014-0056-y]
12. Bouchami O, Achour W, Mekni MA, Rolo J, Ben Hassen A. Antibiotic resistance and molecular characterization of clinical isolates of methicillin-resistant coagulase-negative staphylococci isolated from bacteremic patients in oncohematology. Folia Microbiol. 2011;56(2):122-30. [Link] [DOI:10.1007/s12223-011-0017-1]
13. Rodriguez-Aranda A, Daskalaki M, Villar J, Sanz F, Otero JR, Chaves F. Nosocomial spread of linezolid-resistant Staphylococcus haemolyticus infections in an intensive care unit. Diagn Microbiol Infect Dis. 2009;63(4):398-402. [Link] [DOI:10.1016/j.diagmicrobio.2008.12.008]
14. Froggatt JW, Johnston JL, Galetto DW, Archer GL. Antimicrobial resistance in nosocomial isolates of Staphylococcus haemolyticus. Antimicrob Agents Chemother 1989;33(4):460-6. [Link] [DOI:10.1128/AAC.33.4.460]
15. Ahmed A, Satti L, Zaman G, Gardezi A, Sabir N, et al. Catheter related recurrent blood stream infection caused by linezolid-resistant, methicillin resistant Staphylococcus haemolyticus; an emerging super bug. J Pak Med Assoc. 2019;69(2):261-3. [Link]
16. Eltwisy HO, Twisy HO, Hafez MH, Sayed IM, El-Mokhtar MA. Clinical infections, antibiotic resistance, and pathogenesis of Staphylococcus haemolyticus. Microorganisms. 2022;10(6):1130. [Link] [DOI:10.3390/microorganisms10061130]
17. Silva PV, Cruz RS, Keim LS, de Paula GR, Carvalho BTF, et al. The antimicrobial susceptibility, biofilm formation and genotypic profiles of Staphylococcus haemolyticus from bloodstream infections. Mem Inst Oswaldo Cruz. 2013;108(6):812-3. [Link] [DOI:10.1590/0074-0276108062013022]
18. Rossi CC, Santos-Gandelman JF, Barros EM, Alvarez VM, Laport MS, et al. Staphylococcus haemolyticus as a potential producer of biosurfactants with antimicrobial, anti-adhesive and synergistic properties. Lett Appl Microbiol. 2016;63(3):215-21. [Link] [DOI:10.1111/lam.12611]
19. Takeuchi F, Watanabe S, Baba T, Yuzawa H, Ito T, et al. Whole-genome sequencing of staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol. 2005;187(21):7292-308. [Link] [DOI:10.1128/JB.187.21.7292-7308.2005]
20. Otto M. Staphylococcus colonization of the skin and antimicrobial peptides. Expert Rev Dermatol. 2010;5(2):183-95. [Link] [DOI:10.1586/edm.10.6]
21. Bora P, Datta P, Gupta V, Singhal L, Chander J. Characterization and antimicrobial susceptibility of coagulase-negative staphylococci isolated from clinical samples. J Lab Physicians. 2018;10(4):414-9. [Link] [DOI:10.4103/JLP.JLP_55_18]
22. Khatoon R, Jahan N. Evaluation of prevalence of inducible clindamycin resistance among Coagulase Negative Staphylococci (CoNS) isolated from various clinical samples in a tertiary care hospital of North India. Int J Curr Microbiol Appl Sci. 2018;7(2):513-22. [Link] [DOI:10.20546/ijcmas.2018.702.065]
23. Chika E, Joseph NF, Chijioke E, Peter E. Detection of constitutive- and inducible-clindamycin-resistance in clinical isolates of Staphylococcus aureus from a federal teaching hospital in Abakaliki, Nigeria. J Bacteriol Infect Dis. 2018;2(1):31-4. [Link]
24. Fiebelkorn KR, Crawford SA, McElmeel ML, Jorgensen JH. Practical disk diffusion method for detection of inducible clindamycin resistance in Staphylococcus aureus and coagulase-negative staphylococci. J Clin Microbiol. 2003;41(10):4740-4. [Link] [DOI:10.1128/JCM.41.10.4740-4744.2003]
25. Gatermann SG, Koschinski T, Friedrich S. Distribution and expression of macrolide resistance genes in coagulase-negative staphylococci. Clin Microbiol Infect. 2007;13(8):777-81. [Link] [DOI:10.1111/j.1469-0691.2007.01749.x]
26. Malek-Jafarian M, Hosseini F, Ahmadi A. Pattern of infection and antibiotic activity among Streptococcus agalactiae isolates from adults in Mashhad, Iran. Rep Biochem Mol Biol. 2015;3(2):89-93. [Link]
27. Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin Microbiol Rev. 2014;27(4):870-926. [Link] [DOI:10.1128/CMR.00109-13]
28. Manoharan M, Sistla S, Ray P. Prevalence and molecular determinants of antimicrobial resistance in clinical isolates of Staphylococcus haemolyticus from India. Microb Drug Resist. 2021;27(4) : 501-8. [Link] [DOI:10.1089/mdr.2019.0395]
29. Bouchami O, de Lencastre H, and Miragaia M. Impact of insertion sequences and recombination on the population structure of Staphylococcus haemolyticus. PLoS One. 2016;11(6):e0156653. [Link] [DOI:10.1371/journal.pone.0156653]
30. Barros EM, Ceotto H, Bastos MCF, Dos Santos KRN, Giambiagi-Demarval M. Staphylococcus haemolyticus as an important hospital pathogen and carrier of methicillin resistance genes. J Clin Microbiol. 2012;50(1):166-8. [Link] [DOI:10.1128/JCM.05563-11]
31. Cavanagh JP, Hjerde E, Holden MTG, Kahlke T, Klingenberg C, et al. Whole-genome sequencing reveals clonal expansion of multiresistant Staphylococcus haemolyticus in European hospitals. J Antimicrob Chemother. 2014;69(11):2920-7. [Link] [DOI:10.1093/jac/dku271]
32. Hope R, Livermore DM, Brick G, Lillie M, Reynolds R, et al. Non-susceptibility trends among staphylococci from bacteraemias in the UK and Ireland, 2001-2006. J Antimicrob Chemother. 2008;62 Suppl 2:ii65-74. [Link] [DOI:10.1093/jac/dkn353]
33. Freney J, Kioos WE, Hajek V, Webster JA, Bes M, et al. Recommended minimal standards for description of new staphylococcal species. Int J Syst Bacteriol. 1999;49 Pt 2: 489-502. [Link] [DOI:10.1099/00207713-49-2-489]
34. Clinical & Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. 28th Edition. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute; 2018. [Link]
35. Murakami K, Minamide W, Wada K, Nakamura, E, Teraoka H, Watanabe S. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol. 1991;29(10):2240-4. [Link] [DOI:10.1128/jcm.29.10.2240-2244.1991]
36. Lina G, Quaglia A, Reverdy M, Leclercq R, Vandenesch F, Etienne J. Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci. Antimicrob Agents Chemother. 1999;43(5):1062-6. [Link] [DOI:10.1128/AAC.43.5.1062]
37. Sanches IS, Mato R, de Lancastre H, Tomsaz A. Patterns of multidrug resistance among methicillin-resistant hospital isolates of coagulase-positive and coagulase-negative Staphylococci collected in the international multicenter study RESIST in 1997 and 1998. Microb Drug Resist. 2000;6(3):199-211. [Link] [DOI:10.1089/mdr.2000.6.199]
38. Gaudioso de Allori MC, Jure MA, Romero C, de Castillo ME. Antimicrobial resistance and production of biofilms in clinical isolates of coagulase-negative Staphylococcus strains. Biol Pharm Bull. 2006;29(8):1592-6. [Link] [DOI:10.1248/bpb.29.1592]
39. Mack D, Rohde H, Harris LG, Davies AP , Horstkotte MA, Knobloch JK. Biofilm formation in medical device-related infection. Int J Artif Organs. 2006;29(4):343-59. [Link] [DOI:10.1177/039139880602900404]
40. Kitti T, Seng R, Saiprom N, Thummeepak R, Chantratita N, et al. Molecular characteristics of methicillinresistant staphylococci clinical isolates from a tertiary Hospital in Northern Thailand. Can J Infect Dis Med Microbiol. 2018;2018:8457012. [Link] [DOI:10.1155/2018/8457012]
41. Debnath A, Ghosh R , Ghosh D. Detection of inducible clindamycin resistance (iMLSB) among the erythromycin resistant CoNS isolates in a rural tertiary care hospital- need of time. Int JHealth Sci Res. 2020;10(6):12-18. [Link]
42. Bansal N, Chaudhary U, and Gupta V. Prevalence of inducible clindamycin resistance in clinical isolates of coagulase negative staphylococci at a tertiary care hospital. Ann Trop Med Public Health. 2012;5(5):427-30. [Link] [DOI:10.4103/1755-6783.105124]
43. Perez LRR, Caierão J, Antunes ALS, d'Azevedo PA. Use of the D test method to detect inducible clindamycin resistance in coagulase negative staphylococci (CoNS). Braz J Infect Dis. 2007;11(2):186-8. [Link] [DOI:10.1590/S1413-86702007000200002]
44. Jorgensen JH, Crawford SA, McElmeel ML, Fiebelkorn KR. Detection of inducible clindamycin resistance of staphylococci in conjunction with performance of automated broth susceptibility testing. J Clin Microbiol. 2004;42(4):1800-2. [Link] [DOI:10.1128/JCM.42.4.1800-1802.2004]
45. Teeraputon S, Santanirand P, Wongchai T, Songjang1 W, Lapsomthob N, et al. Prevalence of methicillin resistance and macrolide-lincosamide- streptogramin B resistance in Staphylococcus haemolyticus among clinical strains at a tertiary-care hospital in Thailand. New Microbes New Infect. 2017;19:28-33. [Link] [DOI:10.1016/j.nmni.2017.05.007]
46. Dziri R, Klibi N, Lozano C, Ben Said L, Bellaaj R, Tenorio C, Boudabous A, et al. High prevalence of Staphylococcus haemolyticus and Staphylococcus saprophyticus in environmental samples of a Tunisian hospital. Diagn Microbiol Infect Dis. 2016;85(2):136-40. [Link] [DOI:10.1016/j.diagmicrobio.2016.03.006]

Add your comments about this article : Your username or Email:
CAPTCHA