Bacterial etiology and antimicrobial resistance trends in ocular infections: A 30-year study,Turin area,Italy

Abstract

Purpose:

Bacterial ocular infections can result in loss of all or part of the ocular structures, contributing to a high disability charge. Local surveillance of etiology and susceptibility patterns is crucial for an appropriate empiric management of ocular infections. The aim of this study was to analyze of bacterial spectrum in culture-proven ocular infections and trends of antimicrobial susceptibility patterns.

Methods:

A monocentric retrospective study was performed including ocular infection cases diagnosed at the Microbiology Unit of Turin Ophthalmic Hospital between 1988 and 2017. Spectrum of pathogens that caused bacterial culture-proven ocular infections and trends of antimicrobial susceptibility patterns were analyzed.

Results:

A total of 15,517 culture-positive isolates were identified as causative agents of ocular infections. Gram-positive bacteria were deemed to cause infection in 73.5% of cases. Staphylococcus spp. and Pseudomonas spp., coagulase-negative staphylococci, Staphylococcus aureus were the leading causative pathogens of keratitis, endophthalmitis, and conjunctivitis, respectively. Statistically significant changes in temporal trends were observed for all analyzed microorganism groups except for Enterobacteriaceae group. Overall, fluoroquinolones and chloramphenicol demonstrated to be the most effective antimicrobials in vitro toward bacterial ocular infections, followed by tetracycline, ampicillin, and aminoglycosides. Enterobacteriaceae isolates showed higher multi-drug resistance rate, followed by coagulase-negative staphylococci. Analysis of resistance rates over time highlighted increasing resistance trend for aminoglycosides among Gram-negative and for both aminoglycosides and fluoroquinolones among Gram-positive pathogens, especially for S. aureus.

Conclusion:

This study provided a 30-year assessment of bacterial ocular infections in an urban area of Italy, giving support to epidemiological consciousness and guiding empiric antimicrobial therapy.

Keywords

Ocular infection bacterial epidemiology antimicrobial resistance Gram-positive Gram-negative multi-drug resistance

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References

Buznach

Dagan

Greenberg

Clinical and bacterial characteristics of acute bacterial conjunctivitis in children in the antibiotic resistance era. Pediatr Infect Dis J 2005; 24(9): 823–828.

Leung

AKC

Hon

Wong

AHC

, et al. Bacterial conjunctivitis in childhood: etiology, clinical manifestations, diagnosis, and management. Recent Pat Inflamm Allergy Drug Discov 2018; 12(2): 120–127.

Azari

Barney

NP.

Conjunctivitis: a systematic review of diagnosis and treatment. JAMA 2013; 310(16): 1721–1729.

Austin

Lietman

Rose-Nussbaumer

Update on the management of infectious keratitis. Ophthalmology 2017; 124(11): 1678–1689.

Clarke

Williamson

Gini

, et al. Management of bacterial postoperative endophthalmitis and the role of vitrectomy. Surv Ophthalmol 2018; 63(5): 677–693.

Shimizu

Toshida

Honda

, et al. Prevalence of drug resistance and culture-positive rate among microorganisms isolated from patients with ocular infections over a 4-year period. Clin Ophthalmol 2013; 7: 695–702.

Tam

ALC

Cote

Saldanha

, et al. Bacterial keratitis in Toronto: a 16-year review of the microorganisms isolated and the resistance patterns observed. Cornea 2017; 36(12): 1528–1534.

Lam

Houang

Fan

, et al. Hong Kong microbial keratitis study group. Incidence and risk factors for microbial keratitis in Hong Kong: comparison with Europe and North America. Eye 2002; 16: 608–618.

Sun

Deng

, et al. Distribution and shifting trends of bacterial keratitis in north China (1989–98). Br J Ophthalmol 2004; 88(2): 165–166.

10.

Ting

DSJ

Settle

Morgan

, et al. A 10-year analysis of microbiological profiles of microbial keratitis: the North East England Study. Eye 2018; 32: 1416–1417.

11.

Tena

Rodriguez

Toribio

, et al. Infectious keratitis: microbiological review of 297 cases. Jpn J Infect Dis 2019; 72(2): 121–123.

12.

Ferreira

Figueira

Moreira-Goncalves

, et al. Clinical and microbiological profile of bacterial microbial keratitis in a Portuguese tertiary referral center—where are we in 2015. Eye Contact Lens 2018; 44(1): 15–20.

13.

Orlans

Hornby

Bowler

IC.

In vitro antibiotic susceptibility patterns of bacterial keratitis isolates in Oxford, UK: a 10-year review. Eye 2011; 25: 489–493.

14.

Tan

Walkden

, et al. Twelve-year analysis of microbial keratitis trends at a UK tertiary hospital. Eye 2017; 31(8): 1229–1236.

15.

Peng

Cevallos

McLeod

, et al. Bacterial keratitis: isolated organisms and antibiotic resistance patterns in San Francisco. Cornea 2018; 37(1): 84–87.

16.

Mun

Kim

JY.

Ten-year analysis of microbiological profile and antibiotic sensitivity for bacterial keratitis in Korea. PLoS ONE 2019; 14(3): e0213103.

17.

Sand

She

Shulman

, et al. Microbial keratitis in Los Angeles: the Doheny Eye Institute and the Los Angeles County Hospital experience. Ophthalmology 2015; 122(5): 918–924.

18.

Yang

Liu

Huang

, et al. Clinical analysis of 1593 patients with infectious endophthalmitis: a 12-year study at a tertiary referral center in Western China. Chin Med J 2018; 131(14): 1658–1665.

19.

Mollan

Gao

Lockwood

, et al. Postcataract endophthalmitis: incidence and microbial isolates in a United Kingdom region from 1996 through 2004. J Cataract Refract Surg 2007; 33(2): 265–268.

20.

Carreras

Bacteriological analysis in the management of conjunctivitis. Arch Soc Esp Oftalmol 2012; 87(4): 107–111.

21.

Montagnani

Malandrini

Stolzuoli

, et al. Micro-biological features of acute bacterial conjunctivitis in a central Italian area. New Microbiol 2008; 31(2): 291–294.

22.

Pham

Badenoch

, et al. Bacteria commonly isolated from keratitis specimens retain antibiotic susceptibility to fluoroquinolones and gentamicin plus cephalothin. Clin Exp Ophthalmol 2006; 34(1): 44–50.

23.

Politis

Wajnsztajn

Rosin

, et al. Trends of bacterial keratitis culture isolates in Jerusalem; a 13-years analysis. PLoS ONE 2016; 11(11): e0165223.

24.

Kampitak

Suntisetsin

Sirikul

Clinical and microbiological characteristics of corneal ulcers in a Thai referral center. Asian Biomed 2014; 8: 275–282.

25.

Rahimi

Hashemian

Khosravi

, et al. Bacterial keratitis in a tertiary eye centre in Iran: a retrospective study. Middle East Afr J Ophthalmol 2015; 22(2): 238–244.

26.

Teweldemedhin

Gebreyesus

Atsbaha

, et al. Bacterial profile of ocular infections: a systematic review. BMC Ophthalmol 2017; 17(1): 212.

27.

Khosravi

Mehdinejad

Heidari

Bacteriological findings in patients with ocular infection and antibiotic susceptibility patterns of isolated pathogens. Singapore Med J 2007; 48(8): 741–743.

28.

Saeed

D’Arcy

Stack

, et al. Risk factors, microbiological findings, and clinical outcomes in cases of microbial keratitis admitted to a tertiary referral center in Ireland. Cornea 2009; 28(3): 285–292.

29.

Moloney

Park

Microbiological isolates and antibiotic sensitivities in culture-proven endophthalmitis: a 15-year review. Br J Ophthalmol 2014; 98(11): 1492–1497.

30.

Gupta

Orlans

Hornby

, et al. Microbiology and visual outcomes of culture-positive bacterial endophthalmitis in Oxford, UK. Graefes Arch Clin Exp Ophthalmol 2014; 252(11): 1825–1830.

31.

Celiker

Kazokoglu

Ocular culture-proven endogenous endophthalmitis: a 5-year retrospective study of the microorganism spectrum at a tertiary referral center in Turkey. Int Ophthalmol 2019; 39(8): 1743–1751.

32.

Liu

, et al. Microbiological isolates and antibiotic susceptibilities: a 10-year review of culture-proven endophthalmitis cases. Curr Eye Res 2017; 42(3): 443–447.

33.

Gentile

Shukla

Shah

, et al. Microbiological spectrum and antibiotic sensitivity in endophthalmitis: a 25-year review. Ophthalmology 2014; 121: 1634–1642.

34.

Chen

Adelman

RA.

Microbial spectrum and resistance patterns in endophthalmitis: a 21-year (1988-2008) review in northeast United States. J Ocul Pharmacol Ther 2012; 28(4): 329–334.

35.

Fernández-Rubio

. Re: Gentile et al.: Microbiological spectrum and antibiotic sensitivity in endophthalmitis: a 25-year review (Ophthalmology 2014; 121: 1634–1642). Ophthalmology 2015; 122: e23–4. DOI: 10.1016/j.ophtha.2014.08.050.

36.

Yin

Weisbrod

Eng

, et al. Antibiotic resistance of ocular surface flora with repeated use of a topical antibiotic after intravitreal injection. JAMA Ophthalmol 2013; 131(4): 456–461.

37.

Fintelmann

Hoskins

Lietman

, et al. Topical fluoroquinolone use as a risk factor for in vitro fluoroquinolone resistance in ocular cultures. Arch Ophthalmol 2011; 129(4): 399–402.

38.

Sanfilippo

Morrissey

Janes

, et al. Surveillance of the activity of aminoglycosides and fluoroquinolones against ophthalmic pathogens from Europe in 2010-2011. Curr Eye Res 2016; 41(5): 581–589.

39.

Thomas

Melton

Asbell

PA.

Antibiotic resist-ance among ocular pathogens: current trends from the ARMOR surveillance study (2009-2016). Clin Optom 2019; 11: 15–26.

40.

Morrissey

Burnett

Viljoen

, et al. Surveillance of the susceptibility of ocular bacterial pathogens to the fluoroquinolone gatifloxacin and other antimicrobials in Europe during 2001/2002. J Infect 2004; 49(2): 109–114.

41.

World Health Organization (WHO). Global antimicrobial resistance surveillance system (GLASS) report: early implementation 2016-2017. Geneva: WHO, 2017.

42.

European Centre for Disease Prevention and Control (ECDC). Surveillance of antimicrobial resistance in Europe—Annual report of the European Antimicrobial Resistance Surveillance Network (EARS-Net) 2017. Stockholm: ECDC, 2018.

43.

Asbell

Pandit

Sanfilippo

CM.

Antibiotic resistance rates by geographic region among ocular pathogens collected during the ARMOR surveillance study. Ophthalmol Ther 2018; 7(2): 417–429.