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Clinical science
Queensland Microbial Keratitis Database: 2005–2015
  1. Matthew Green1,2,
  2. Nicole Carnt2,
  3. Andrew Apel3,
  4. Fiona Stapleton2
  1. 1 Ophthalmology department, Gold Coast University Hospital, Southport, Queensland, Australia
  2. 2 School of Optometry and Vision Science, University of New South Wales, Kensington, Queensland, Australia
  3. 3 Ophthalmology department, Princess Alexandra Hospital, Brisbane, Queensland, Australia
  1. Correspondence to Dr Matthew Green, Gold Coast University Hospital, Southport, QLD 4215, Australia; doctormatthewgreen{at}gmail.com

Abstract

Aims To estimate the incidence of culture-positive microbial keratitis in Queensland and analyse trends in the organisms and their sensitivities cultured from corneal scrapes, especially low-incidence organisms.

Methods Retrospective multicentre case series of all positive corneal scrapes in Queensland, Australia between 2005 and 2015. Pathology organisations in Queensland were identified by online and local directory search and agreed to participate. Digital records of scrapes provided patient demographics and culture and susceptibility results. Trends in the incidence, organisms and sensitivities were monitored with linear regression. The yearly incidence of microbial keratitis was estimated from the Queensland population.

Results The included corneal scrapes totalled 3182, while 1006 were excluded. The included scrapes yielded 4111 organisms. Pseudomonas aeruginosa was the most common single isolate (729, 17.7%), although Gram-positive organisms were more common overall (2737, 66.6%). Fungal organisms were cultured in 6% of cases, while Acanthamoeba comprised only 1% of records. Bacterial organisms were sensitive to all recorded antibiotics in 89% of all isolates and none of the reported antibiotics showed a decreasing trend in susceptibility. The incidence of protozoal isolation decreased over time (p=0.055). Cultures positive for yeasts showed a linear increase in incidence (p=0.045) while moulds showed a spike in incidence in 2010–2012 (p=0.0008).

Conclusion The estimated incidence of microbial keratitis was 0.66 cases per 10 000 people, the rate of antibiotic susceptibility is high and stable, the incidence of keratitis secondary to protozoa is likely to be decreasing while the incidence of keratitis culturing yeast is increasing.

  • cornea
  • infection

https://doi.org/10.1136/bjophthalmol-2018-312881

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    Introduction

    Microbial keratitis is an infection of the cornea caused by bacteria, fungal, protozoa and viral organisms. This is characterised by a corneal infiltrate, epithelial defect and anterior chamber reaction, which may result in a high rate of vision loss and/or surgical intervention.1 Treatment of microbial keratitis includes an initial corneal scrape and subsequent empirical antibiotics until confirmation of the infective organism. Corneal scrapes for culture are also used to monitor trends in infective organisms and antibiotic resistance.

    Studies of microbial keratitis in Australia, from Brisbane,1 Adelaide,2 3 Sydney,4–6 Perth7 and Melbourne8 have shown that Gram-positive bacteria (51%–75%) are more common than Gram-negative organisms (22%–48%). The most common organism found in four of these studies has been coagulase-negative staphylococci (CNS, 13%–47%) and Staphylococcus aureus in two other studies (8%–20%). Pseudomonas aeruginosa has been found in 8%–27% and fungi in 4%–9% of cases in these studies. In Australia, there are higher rates of P. aeruginosa culture in warmer (Brisbane)1 compared with cooler southern climates (Melbourne).8 9

    Rates of antibiotic susceptibility in corneal isolates in Australia are generally high. A recent review in Sydney showed high rates of susceptibility to ciprofloxacin in all bacterial species.5 6 Although one study of severe keratitis has found low susceptibility to cephalothin in Gram-positive organisms (23.1%) but conversely, high susceptibility of Gram negatives to gentamicin (84.6%).7 Decreasing sensitivities to cephalothin among Gram-positive organisms have been reported, although the rates of susceptibility are still high (88%).10

    Most epidemiological studies of microbial keratitis describe single-centre studies of microbiological databases/medical records and less frequently conducted population-based incidence studies.11 12 Single-centre studies are important, tend to be of medium length (3–5 years) but only cover a narrow geographical area and cannot define keratitis incidence. Conversely, population-based incidence studies can define incidence, cover a broad area but due to their cost and complexity are short (1 year) and infrequent. Furthermore, because of the short duration or low numbers in studies both study designs have difficulty in evaluating low-incidence disease, such as keratitis caused by fungal, protozoal organisms or antibiotic-resistant bacteria.

    This study is a review of microbiological records from all pathology centres in the state of Queensland, Australia over an 11-year period. This has allowed a review of a large number of cultured organisms and their sensitivities over a long period of time and large geographical area.

    Methods

    The results of positive corneal scrapes of all pathology laboratories in the state of Queensland, Australia between January 2005 and December 2015 were amalgamated.

    Queensland Microbial Keratitis Database

    Pathology organisations in Queensland were identified by online and local directory search. They were approached if it was indicated they carried out microbiological testing. All identified laboratories agreed to participate.

    The four pathology organisations included were:

    1. Queensland Pathology—sole public pathology service for Queensland, 35 laboratories in public hospitals.

    2. Sullivan and Nicolaides Pathology—18 laboratories, 349 collection centres.

    3. Mater Pathology—3 laboratories, 22 collection centres.

    4. Queensland Medical Laboratories—24 laboratories, over 600 collection centres.

    Each organisation supplied lists of positive corneal scrape results. This included deidentified patient demographics (age, sex, home postcode) and culture result and antibiotic susceptibility. Results were analysed for years where all laboratories provided results; 2005–2015. These results were excluded if they included the words: swab, aqueous or vitreous in the site description, they did not have a Queensland postcode or they were a duplicate record.

    Antibiotic susceptibility was filtered to record a specific panel of antibiotics relevant to the management of microbial keratitis. These antibiotics were vancomycin, first and third-generation cephalosporins, second-generation fluoroquinolones (ofloxacin and ciprofloxacin), gentamicin and chloramphenicol.

    Estimated yearly incidence of microbial keratitis in Queensland

    The yearly incidence of microbial keratitis was estimated from the number of records and the population of Queensland in each year. Data from the Australian Bureau of Statistics were used to provide the Queensland population (www.abs.gov.au). The average yearly incidence was calculated from the average number of records and the average Queensland population for the 11-year period 2005–2015. This will represent the culture-positive microbial keratitis in Queensland, but will not include the culture-negative keratitis or the cases managed without corneal culture.

    Trends over time were evaluated by linear regression of yearly incidence. This was carried out for the incidence of total rate of microbial keratitis, cultures positive for each organism group and bacterial antibiotic resistance. If organisms showed a non-linear trend, this was analysed by a χ2 test of the peak years to other years. Organisms that demonstrated a statistically significant trend were further analysed to illicit more information on the nature of the change in trend. For each organism group: average age, sex, geographic distribution and rate of urban postcode were compared between the periods of high and low rates of organism culture.

    The geographic distribution of the data set was categorised into four groups according to the latitude of the patient’s home postcode. These were group 1: −10° to −15°, group 2: −15° to −20°, group 3: −20° to −25° and group 4: −25° to −30°. The rural, remote, metropolitan area (RRMA) index was also used to classify the area patients lived in. This index is based on population figures and statistical local area boundaries. Patients were deemed to live in an urban postcode if the RRMA of their postcode was 1–2 (capital city or other metropolitan area) and regional/rural if it was 3–7 (large rural centre to remote centre/area).13

    All p values listed are χ2 tests unless stated otherwise. Data were analysed with SPSS V.24.0 (IBM) and Stata V.15 (StataCorp, Texas, USA).

    Results

    There were 3182 eligible corneal scrapes included. An additional 1006 records were identified but excluded because they indicated the patients lived interstate, overseas or their postcode was not recorded; their record indicated aqueous, vitreous or swab or their culture was outside the study period of 2005–2015.

    The average age of patients in included records was 53 years (SD 22.6) and there was a slight predominance of male patients (1670, 52.4%) in the eligible records.

    Microbiology results

    The 3182 patient records included yielded 4111 organisms. Multiple organisms were found in 763 (23.97%) records. The most common single organism recovered was P. aeruginosa. It was cultured in 729 (17.7%) patients, although Gram-positive organisms were more common overall (2737, 66.6%; table 1). Fungal organisms were cultured in 6% of cases, while A canthamoeba comprised only 1% of records.

    View this table:
    Table 1

    Cultured organisms and antibiotic susceptibility

    Estimated incidence of culture-positive microbial keratitis

    The average estimated incidence of culture-positive microbial keratitis in Queensland between 2005 and 2015 was 0.66 cases per 10 000 people (95% CI 0.65 to 0.67). The incidence was calculated from the average number of cases per year (289) and the average population in Queensland during the study (4 380 513).

    The average yearly incidence of fungal keratitis was 0.052 per 10 000 people (95% CI 0.043 to 0.060) while the average yearly incidence of A canthamoeba keratitis was 0.005 cases per 10 000 people (95% CI 0.0026 to 0.0073).

    Organism susceptibility

    Bacterial organisms were sensitive to all recorded antibiotics in 89% of all isolates. There was no decreasing trend in susceptibility to any of the reported antibiotics (figure 1). In fact, the number of cases sensitive to first-generation cephalosporins and chloramphenicol (p=0.053) increased. Antibiotic resistance was most common to first-generation cephalosporins and resistance was more common in Gram-positive organisms (table 1).

    Figure 1
    Figure 1

    Longitudinal trends in percentage of tested organisms resistant to recorded antibiotics.

    Resistance to second-generation fluoroquinolones was found in 96 organisms (4%). These were mostly CNS, although three cultures of P. aeruginosa were also resistant (0.4%). These three cases were sporadic and had no geographic or chronological association.

    Longitudinal trends in culture results

    The annual estimated incidence of microbial keratitis in Queensland between 2005 and 2015 varied from 0.552 to 0.753 per 10 000 people (figure 2). Linear regression of the annual incidence showed a mild but non-significant increase over the duration of the study (table 2, p=0.125).

    Figure 2
    Figure 2

    Estimated incidence of cultured organisms (n per 10 000 people).

    View this table:
    Table 2

    Linear regression of longitudinal trend in different patient groups

    This mild increase was also the case for Gram-positive organisms; however, Gram-negative organisms remained stable during the study (figure 2, table 2). The increase in Gram-positive organisms was mainly evident in CNS which did show a mild but significant increase.

    The incidence of fungal recovery similarly showed a non-significant increase over the course of the study (figure 3, table 2). However, this can be separated into moulds which showed a significant spike in their incidence between 2010 and 2012 (0.057/10 000 people vs other years 0.035/10 000 people; p=0.0008) whereas yeasts showed a linear increase in their rate of recovery.

    Figure 3
    Figure 3

    Estimated incidence of low-incidence cultured organisms (n per 10 000 people).

    Further analysis of the fungi showed that yeasts had a statistically significant increase throughout the study, while moulds (filamentous fungi) showed a temporary increase in the yearly incidence during the years 2010–2012.

    In the patients with mould or yeast isolated from their corneal scrape there was no difference in the average age, geographic distribution (latitude groups), urban postcodes or sex distribution between the periods of high and low rates of culture. These differences in patients that cultured mould were compared between the peak of 2010–2012 versus other years; while differences in patients with yeast culture were tested between the first and second half of the study with χ2 tests.

    Protozoa showed an almost significant decrease in incidence throughout the study (figure 3, table 2).

    Discussion

    This study has shown that the average estimated incidence of culture-positive microbial keratitis in Queensland between 2005 and 2015 was 0.66 cases (95% CI 0.65 to 0.67) per 10 000 people. It has also shown that the majority of the cultured organisms were Gram-positive bacteria, while P. aeruginosa was the single most common isolate. Fungal organisms represented about 6% of all isolates and protozoa were rarely isolated.

    The incidence of keratitis in this study is similar to a study in Hong Kong in 2002 which found 0.63 per 10 00014 but higher than a study in Scotland in 1999 which found only 0.26 per 10 000.12 Comparison to these two studies is limited by differing inclusion criteria. Our study and the Scottish study used culture-proven keratitis while the Hong Kong study used a clinical assessment of keratitis. Our study does not include culture-negative keratitis and ophthalmologist management of keratitis without corneal scrape for culture is not included in our study.

    A study in Northern California has also used collaborative data identified through their outpatient diagnostic database to analyse the incidence of keratitis. In their population they found that 2.76 patients per 10 000 person-years had ulcerative keratitis. The main reason for the 3× difference in the estimated incidence is that they included culture-negative cases. In fact, only 10% of the included 300 patients had a positive corneal culture.15

    This study has shown a mild increase in Gram-positive organisms but stable Gram-negative organism rates over the 11-year period. These results from Queensland do not reflect the significant increase in Gram-positive bacteria over time found in Taiwan16 and Toronto17 or Gram-negative bacteria in Kent, UK.18

    The rate of fungal keratitis in Australia has been reported to be between 3.7% and 9% of all isolates.1–7 This can be compared with very high rates of fungal isolation from studies in India (32.1%–76.8%).19 The spike in incidence of F usarium keratitis (and other moulds) in this study has occurred after the spike in F usarium infections related to ReNu contact lens solutions in 2005–2008 seen in other countries.20 21 It has also occurred before the recent increasing rate of contact lens-related Fusarium keratitis revealed in London.22

    There was a twofold change in incidence of corneal yeast infections over time in this population. Subgroup analysis of patients did not show any shift in age group, urban dwelling or longitudinal distribution between the first and second half of the study. This suggests that the trend seen in these data reflects an expansion of an existing pattern of disease, rather than a shift in the epidemiological characteristics of patients with yeast infections.

    The average incidence of fungal keratitis in this study was 0.052/10 000 population. This is significantly higher than the estimated incidence of fungal keratitis in the UK of 0.003/10 000 population in 200923 and in Denmark of 0.006/10 000 population in 2015.24 This 9–18× difference in the incidence is potentially related to the tropical climate of Queensland compared with the temperate climate of the UK and Denmark. These other studies have also described their estimated incidences as the minimal estimated incidence due to the potentially incomplete methods of disease capture that were used (questionnaire and medical record review, respectively).

    The average yearly incidence of A canthamoeba keratitis was low (0.005 per 10 000 people) and is likely to be decreasing. This decreasing trend comes after a local cluster of infections in 2008 which has been previously reported.25 This reducing incidence does not reflect the increasing rate of ‘resurgent’ Acanthamoeba in New Zealand which has been recently reported.26

    The rate of antibiotic susceptibility among cultured bacteria in this study was high and remained stable through the study period. It has not confirmed the decreasing susceptibility to cephalosporins previously reported in this population10 and in South Australia.2 It has also found higher rates of antibiotic susceptibility than that seen in older patients5 or severe keratitis7 in other Australian studies.

    Fluoroquinolone susceptibility in this study (96%) was high and did not show the decreasing trend seen elsewhere in the world.27 Additionally the susceptibility of P. aeruginosa to fluoroquinolone was very high (99.6%) and higher than the average worldwide susceptibility of 90.9%.28 However, it is important to realise that resistance to fluoroquinolones does exist with occasional cases of P. aeruginosa resistance, although it is not common, and there is no evidence it is increasing.

    This study has benefited greatly from the centralisation of microbiological services in Queensland. This centralisation also gives the study an extremely high likelihood of close to 100% inclusion. However, the possibility of missed records due to closed microbiology practices exists and this inclusion rate cannot be guaranteed. Also, the study is retrospective and cannot plan for differences or changes in culture or susceptibility techniques.

    Inclusion of a large number of records over a long period of time and a large geographical area has offered a thorough longitudinal analysis of the infective organisms and their antibiotic sensitivities in the region.

    Acknowledgments

    Queensland Microbial Keratitis Database contributors: Professor Graeme Nimmo, MBBS, MSc, MPH, MD, PRCPA, FASM, Pathology Queensland, Graeme.nimmo@health.qld.gov.au, Dr Jenny Robson, FRACP, FRCPA, FACTM, Sullivan Nicolaides Pathologists; jenny_robsn@snp.com.au, Dr Sanmarie Schlebusch, MBChB, AMC Cert, FRCPA, Mater Pathology; sanmarie.schlebusch@mater.org.au, Dr Renu Vohra, MBBS, FRCPA, Queensland Medical Laboratories; drrenu.vohra@qml.com.au and Dr Sanmarie Schlebusch for her assistance in fungal species classification.

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    Footnotes

    • Contributors All authors have contributed significantly to the writing of this article. MG conceived the project; designed the study; acquired, analysed and interpreted the data; and drafted and revised the paper. NC helped acquire the data and revise the paper. AA helped design the study, interpret the data and revise the paper. FS helped conceive and design the study, interpret the data and revise the paper. All authors gave final paper approval for submission and agree to be accountable for all aspects of the paper.

    • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

    • Competing interests None declared.

    • Patient consent for publication Not required.

    • Ethics approval This study was approved by the Princess Alexandra Human Research Ethics Committee.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Data sharing statement Data sharing will be considered on application.

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