Kosin Med J.  2024 Jun;39(2):112-119. 10.7180/kmj.23.152.

Statins as a possible factor affecting fluoroquinolone resistance of coagulase-negative Staphylococcus in the conjunctiva: a case-control study

• Hong YR
• Oh CE
• Lee SJ

• KMID: 2556808
• DOI: http://doi.org/10.7180/kmj.23.152

Abstract

Background
Conjunctival bacterial flora is a common cause of endophthalmitis after ophthalmic procedures. This study investigated the conjunctival bacterial flora, especially coagulase-negative Staphylococcus (CoNS), and their antibiotic sensitivity in patients who underwent ophthalmic procedures. Factors related to fluoroquinolone resistance were also investigated.
Methods
In total, 167 samples were analyzed from 135 patients who underwent cataract surgery or intravitreal injection at Kosin University Gospel Hospital between April 14, 2014, and September 29, 2016. Bacterial identification was performed using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry or VITEK 2 equipment. Antibiotic sensitivity tests were performed using an AST-P600 card with VITEK 2 equipment. Clinical information was extracted from patients’ medical records. Sixty-eight individuals with conjunctival flora containing CoNS were classified into the fluoroquinolone-sensitive and fluoroquinolone-resistant CoNS groups, and their characteristics were compared.
Results
A total of 192 isolates of Gram-positive bacteria were identified, including Staphylococcus epidermidis (33.3%), Corynebacterium spp. (18.8%), and CoNS other than S. epidermidis (9.2%). Of the 106 CoNS isolates, 68.9%, 69.8%, and 58.5% were sensitive to ciprofloxacin, levofloxacin, and norfloxacin, respectively. In patients with CoNS, statin use within 3 months before sample collection was significantly associated with fluoroquinolone resistance (p=0.016). Statin use was a significant risk factor for fluoroquinolone resistance in multivariate logistic regression analysis (odds ratio, 4.86; 95% confidence interval, 1.25–18.91; p=0.022).
Conclusions
CoNS, including S. epidermidis, was the most common conjunctival bacterial flora, with a fluoroquinolone sensitivity rate ranging from 58.5% to 69.8% in patients undergoing ophthalmic procedures. Statin use was a significant risk factor for fluoroquinolone resistance.

Keyword

Cataract surgery; Conjunctival bacterial flora; Fluoroquinolone resistance; Intravitreal injections; Statin

Reference

References

1. Grzybowski A, Brona P, Kim SJ. Microbial flora and resistance in ophthalmology: a review. Graefes Arch Clin Exp Ophthalmol. 2017; 255:851–62.

2. McDonald M, Blondeau JM. Emerging antibiotic resistance in ocular infections and the role of fluoroquinolones. J Cataract Refract Surg. 2010; 36:1588–98.

3. Speaker MG, Milch FA, Shah MK, Eisner W, Kreiswirth BN. Role of external bacterial flora in the pathogenesis of acute postoperative endophthalmitis. Ophthalmology. 1991; 98:639–50.

4. Lin YH, Kang YC, Hou CH, Huang YC, Chen CJ, Shu JC, et al. Antibiotic susceptibility profiles of ocular and nasal flora in patients undergoing cataract surgery in Taiwan: an observational and cross-sectional study. BMJ Open. 2017; 7:e017352.

5. Gentile RC, Shukla S, Shah M, Ritterband DC, Engelbert M, Davis A, et al. Microbiological spectrum and antibiotic sensitivity in endophthalmitis: a 25-year review. Ophthalmology. 2014; 121:1634–42.

6. Mino de Kaspar H, Koss MJ, He L, Blumenkranz MS, Ta CN. Antibiotic susceptibility of preoperative normal conjunctival bacteria. Am J Ophthalmol. 2005; 139:730–3.

7. Park SH, Lim JA, Choi JS, Kim KA, Joo CK. The resistance patterns of normal ocular bacterial flora to 4 fluoroquinolone antibiotics. Cornea. 2009; 28:68–72.

8. Lee J, Choi S. Risk factors for fluoroquinolone resistance in ocular cultures. Korean J Ophthalmol. 2015; 29:7–13.

9. Graziano TS, Cuzzullin MC, Franco GC, Schwartz-Filho HO, de Andrade ED, Groppo FC, et al. Statins and antimicrobial effects: simvastatin as a potential drug against Staphylococcus aureus biofilm. PLoS One. 2015; 10:e0128098.

10. Ko HH, Lareu RR, Dix BR, Hughes JD. Statins: antimicrobial resistance breakers or makers? PeerJ. 2017; 5:e3952.

11. Abavisani M, Hoseinzadeh M, Khayami R, Kodori M, Soleimanpour S, Sahebkar A. Statins, allies against antibiotic resistance? Curr Med Chem 2023 Aug 29 [Epub]. https://doi.org/10.2174/0929867331666230829141301.

12. Wayne PA. Clinical and laboratory standards institute: performance standards for antimicrobial susceptibility testing. Inform Suppl. 2011; 31:100–121.

13. Miller D. Update on the epidemiology and antibiotic resistance of ocular infections. Middle East Afr J Ophthalmol. 2017; 24:30–42.

14. de Kaspar HM, Kreidl KO, Singh K, Ta CN. Comparison of preoperative conjunctival bacterial flora in patients undergoing glaucoma or cataract surgery. J Glaucoma. 2004; 13:507–9.

15. Semanyenzi SE, Abahuje E. Normal conjunctival flora as seen in adult patients at Kigali University Teaching Hospital. Rwanda Med J. 2013; 70:22–4.

16. Olson R, Donnenfeld E, Bucci FA, Price FW, Raizman M, Solomon K, et al. Methicillin resistance of Staphylococcus species among health care and nonhealth care workers undergoing cataract surgery. Clin Ophthalmol. 2010; 4:1505–14.

17. Mshangila B, Paddy M, Kajumbula H, Ateenyi-Agaba C, Kahwa B, Seni J. External ocular surface bacterial isolates and their antimicrobial susceptibility patterns among pre-operative cataract patients at Mulago National Hospital in Kampala, Uganda. BMC Ophthalmol. 2013; 13:71.

18. Capriotti JA, Pelletier JS, Shah M, Caivano DM, Ritterband DC. Normal ocular flora in healthy eyes from a rural population in Sierra Leone. Int Ophthalmol. 2009; 29:81–4.

19. Gunduz G, Gunduz A, Polat N, Cumurcu BE, Yakupogullari Y. The effect of chronic alcoholism on the conjunctival flora. Curr Eye Res. 2016; 41:734–9.

20. Suto C, Morinaga M, Yagi T, Tsuji C, Toshida H. Conjunctival sac bacterial flora isolated prior to cataract surgery. Infect Drug Resist. 2012; 5:37–41.

21. Ta CN, Chang RT, Singh K, Egbert PR, Shriver EM, Blumenkranz MS, et al. Antibiotic resistance patterns of ocular bacterial flora: a prospective study of patients undergoing anterior segment surgery. Ophthalmology. 2003; 110:1946–51.

22. Graham JE, Moore JE, Jiru X, Moore JE, Goodall EA, Dooley JS, et al. Ocular pathogen or commensal: a PCR-based study of surface bacterial flora in normal and dry eyes. Invest Ophthalmol Vis Sci. 2007; 48:5616–23.

23. Papa V, Blanco AR, Santocono M. Ocular flora and their antibiotic susceptibility in patients having cataract surgery in Italy. J Cataract Refract Surg. 2016; 42:1312–7.

24. Hoshi S, Hashida M, Urabe K. Risk factors for aerobic bacterial conjunctival flora in preoperative cataract patients. Eye (Lond). 2016; 30:1439–46.

25. Park HJ, Yi GY, Moon NJ. Bacteriologic study on normal conjunctival flora and change of antibiotic susceptability. J Korean Ophthalmol Soc. 2001; 42:817–24.

26. Haas W, Pillar CM, Torres M, Morris TW, Sahm DF. Monitoring antibiotic resistance in ocular microorganisms: results from the Antibiotic Resistance Monitoring in Ocular Microrganisms (ARMOR) 2009 surveillance study. Am J Ophthalmol. 2011; 152:567–74.

27. Asbell PA, Sanfilippo CM, Pillar CM, DeCory HH, Sahm DF, Morris TW. Antibiotic resistance among ocular pathogens in the United States: five-year results from the Antibiotic Resistance Monitoring in Ocular Microorganisms (ARMOR) surveillance study. JAMA Ophthalmol. 2015; 133:1445–54.

28. Hsu HY, Lind JT, Tseng L, Miller D. Ocular flora and their antibiotic resistance patterns in the midwest: a prospective study of patients undergoing cataract surgery. Am J Ophthalmol. 2013; 155:36–44.

29. Lu LJ, Liu J. Human microbiota and ophthalmic disease. Yale J Biol Med. 2016; 89:325–30.

30. Dong Q, Brulc JM, Iovieno A, Bates B, Garoutte A, Miller D, et al. Diversity of bacteria at healthy human conjunctiva. Invest Ophthalmol Vis Sci. 2011; 52:5408–13.

31. Sharma S. Antibiotic resistance in ocular bacterial pathogens. Indian J Med Microbiol. 2011; 29:218–22.