Clinical and Microbiological Analysis of Gram-Positive Bacterial Keratitis, a 15-Year Review

Mi Rae Kim; Sang Bumm Lee

doi:10.3341/jkos.2014.55.10.1432

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Kim and Lee: Clinical and Microbiological Analysis of Gram-Positive Bacterial Keratitis, a 15-Year Review

Original Article

J Korean Ophthalmol Soc 2014;55(10):1432-1444.

Published online: 2 September 2014

DOI: https://doi.org/10.3341/jkos.2014.55.10.1432

Clinical and Microbiological Analysis of Gram-Positive Bacterial Keratitis, a 15-Year Review

Mi Rae Kim, MD, Sang Bumm Lee, MD, PhD

Department of Ophthalmology, Yeungnam University College of Medicine, Daegu, Korea

Address reprint requests to Sang Bumm Lee, MD, PhD, Department of Ophthalmology, Yeungnam University Medical Center, #170 Hyeonchung-ro, Nam-gu, Daegu 705-802, Korea, Tel: 82-53-620-3445, Fax: 82-53-626-5936 E-mail: sbummlee@ynu.ac.kr

Received 16 May 2014 Revised 2 July 2014 Accepted 3 October 2014

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Purpose

To investigate the shifting trends of pathogenic organisms, antibiotic resistance, and clinical characteristics of patients with Gram-positive bacterial keratitis and to elucidate the prognostic factors.

Methods

We performed a retrospective chart review of 152 isolates in 146 eyes with Gram-positive bacterial keratitis between January 1998 and December 2012. The study was divided into 5 periods for analysis of the bacteriological profiles and in vitro antibiotic resistance. The epidemiological and clinical characteristics were compared according to bacterial isolates. Logistic regression analysis was performed to determine the risk factors.

Results

Gram-positive bacterial keratitis tended to decrease and significant change in the distribution of isolates was not observed. Commonly isolated organisms were S. epidermidis (48.7%), S. aureus (25.0%), and S. pneumoniae (7.2%) in order of frequency. The resistance to fluoroquinolone tended to increase (p = 0.104) and resistance to gentamicin was significantly decreased (p = 0.01). S. epidermidis had the shortest corneal epithelium healing time (p = 0.035) and the most favorable visual outcome after treatment (p = 0.035) compared with the other species. Risk factors for poor visual outcomes included a best corrected visual acuity less than 0.1 at initial evaluation and an epithelial healing time greater than 10 days.

Conclusions

Gram-positive bacterial keratitis tended to decrease and S. epidermidis was the most common isolate. The clinical prognosis was most favorable in S. epidermidis. The BCVA less than 0.1 at initial evaluation was an important risk factor for poor visual outcome and surgical treatment in Gram-positive bacterial keratitis.

Keywords: Enterococcus species, Gram-positive bacterial keratitis, Staphylococcus aureus, Staphylococcus epidermidis, Streptococcus species

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Figure 1.

Prevalence of Gram-positive bacterial isolates in total bacterial keratitis during 1998-2012. The p-value was calculated using chi-square test to com pare the distribution of the Gram-positive bacterial isolates between 2 periods. ^*Gram-positive bacterial isolates significantly decreased between 2 periods.

Figure 2.

Organisms and shifting trend in Gram-positive bacterial isolates during 1998-2012. ^*Six eyes had mixed infection of 2 Gram-positive bacterial species (S. epidermidis & S. aureus (2 eyes), S. epidermidis & E. feacalis, S. epidermidis & S. sanguis, S. aureus & E. feacalis, S. dysgalactiae & S. pyogenes); ^†The p-value was calculated using Spearman rank correlation coefficient to compare the distribution of the bacterial isolates for 15 years. CNS = coagulase-negative Staphylococcus.

Figure 3.

Trends in antimicrobial resistance of Gram-positive bacterial isolates. ^*The resistance of gentamicin decreased significantly (p = 0.01, Spearman rank correlation coefficient); ^†N1 = number of isolates with resistance; N2 = number of tested isolates; ^‡The p-value was calculated using Spearman rank correlation coefficient to compare the distribution of the antimicrobial resistance for 15 years; ^§Total value of fluoroquinolone: ciprofloxacin (n = 70), norfloxacin (n = 21), levofloxacin (n = 25), and moxifloxacin (n = 21).

Figure 4.

Trends in antimicrobial resistance to oxacillin in S. epidermidis and S. aureus. Oxacillin resistance of S. epidermidis was significantly higher than that of S. aureus (p = 0.001, Chi-square test).

Table 1.

Demographics of Gram-positive bacterial keratitis according to the isolated microorganisms

	No. of cases (%)
Characteristics	All case	S. epidermidis	S. aureus	Strepto. spp.	Entero. spp.
	(n = 146)	(n = 74)	(n = 38)	(n = 22)	(n = 16)
Sex (M:F)	1.11:1	1.24:1	1.24:1	1:1	1:1
Age (years)
60≤	68 (46.6)	28 (37.8)^*	20 (52.6)	15 (68.2)	8 (50.0)
40-59	44 (30.1)	29 (39.2)^*	10 (26.3)	2 (9.1)	4 (25.0)
20-39	22 (15.2)	13 (17.6)^*	4 (10.5)	2 (9.1)	3 (18.8)
<20	12 (8.2)	4 (5.4)^*	4 (10.5)	3 (13.6)	1 (6.3)
Seasonal distribution
Spring (Mar-May)	55 (37.7)	28 (37.8)	12 (31.6)	9 (40.9)	7 (43.8)
Summer (Jun-Aug)	27 (18.5)	13 (17.6)	10 (26.3)	2 (9.1)	3 (18.8)
Autumn (Sep-Nov)	30 (20.5)	14 (18.9)	6 (15.8)	7 (31.8)	3 (18.8)
Winter (Dec-Feb)	34 (23.3)	19 (25.7)	10 (26.3)	4 (18.2)	3 (18.8)
Predisposing factors^†
Trauma	53 (36.3)	31 (41.9)	9 (23.7)	9 (40.9)	5 (31.3)
Previous ocular surface disease	45 (30.8)	21 (28.4)	14 (36.8)	7 (31.8)	6 (37.5)
Previous ocular surgery	27 (18.5)	12 (16.2)	8 (21.1)	4 (18.2)	3 (18.8)
Systemic disease	42 (28.8)	17 (23.0)	13 (34.2)	6 (27.3)	6 (37.5)
Contact lens wear	8 (5.5)	5 (6.8)	2 (5.3)	1 (4.5)	1 (6.3)

Strepto. spp. = Streptococcus species; Entero. spp. = Enterococcus species.

^* The p-value was < 0.05, which was calculated for comparison of proportions with all other groups by chi-square test;

^† Sum of the number of eyes with each subgroup does not add up to 100% because of overlap of subgroups and no history of identified predisposing factors.

Table 2.

Clinical characteristics at initial presentation, epithelial healing time, surgical treatment, and visual outcome of Gram-positive bacterial keratitis according to the isolated microorganisms

	No. of cases (%)
Characteristics	All cases	S. epidermidis	S. aureus	Strepto. spp.	Entero. spp.
	(n = 146)	(n = 74)	(n = 38)	(n = 22)	(n = 16)
Corneal lesion
Location^†
Central	91 (62.3)	42 (56.8)	23 (60.5)	17 (77.3)	12 (75.0)
Marginal	55 (37.7)	32 (43.2)	15 (39.5)	5 (22.7)	4 (25.0)
Size
<5 mm²	89 (61.0)	52 (68.4)	23 (60.5)	10 (45.5)	8 (50.0)
≥5 mm²	57 (39.0)	24 (31.6)	15 (39.5)	12 (54.5)	8 (50.0)
Hypopyon
No	105 (71.9)	56 (76.7)	26 (68.4)	14 (63.6)	11 (68.8)
Yes	41 (28.1)	18 (24.3)	12 (31.6)	8 (36.4)	5 (31.3)
Epithelial healing time^‡ (n = 119)	10.8 ± 11.1	8.8 ± 11.1^*	11.8 ± 8.6	13.6 ± 11.9	15.9 ± 14.4
Surgical treatment	22 (15.1)	11 (14.9)	7 (18.4)	4 (18.2)	4 (25.0)
Initial BCVA (Snellen acuity)
<0.1	68 (46.6)	29 (39.2)	19 (50.0)	14 (63.6)	8 (50.0)
0.1-0.5	54 (37.0)	33 (44.6)	14 (36.8)	4 (18.2)	6 (37.5)
0.6-1.0	24 (16.4)	12 (16.2)	5 (13.2)	4 (18.2)	2 (12.5)
Final BCVA (Snellen acuity)
<0.1	44 (30.1)	16 (21.7)^*	14 (36.8)	10 (45.5)	8 (50.0)
0.1-0.5	39 (26.7)	23 (31.1)^*	10 (26.3)	5 (22.7)	2 (12.5)
0.6-1.0	63 (43.2)	35 (47.3)^*	14 (36.8)	7 (31.8)	6 (37.5)

Values are presented as mean ± SD unless otherwise indicated.

Strepto. spp. = Streptococcus species; Entero. spp. = Enterococcus species; BCVA = best corrected visual acuity.

^* The p-value was < 0.05, which was calculated for comparison of proportions with all other groups by independent t-test or chi-square test;

^† ‘Central’ is located within 1/2 radius from the center of the cornea, ‘Marginal’ is located within 1/2 radius from the limbus;

^‡ The eyes were excluded if surgical treatment was done (22 eyes) or the record for epithelial healing time was missed (5 eyes).

Table 3.

Comparisons of epidemiologic and clinical features and treatment outcome between MSS and MRS

Characteristics	No. of cases (%)		p-value^‡
Characteristics	MSS (n = 56)	MRS (n = 56)	p-value^‡
Sex (M:F)	1.24:1	1.24:1	1.000
Age (years)			0.399
60≤	21 (37.5)	27 (48.2)
40-59	21 (37.5)	18 (32.1)
20-39	11 (19.6)	6 (10.7)
<20	3 (5.4)	5 (8.9)
Seasonal distribution			0.377
Spring (Mar-May)	17 (30.4)	23 (41.1)
Summer (Jun-Aug)	14 (25.0)	9 (16.1)
Autumn (Sep-Nov)	12 (21.4)	8 (14.3)
Winter (Dec-Feb)	13 (23.2)	16 (28.6)
Predisposing factors
Trauma	15 (26.8)	25 (44.6)	0.049
Previous ocular surface disease	18 (32.1)	17 (30.4)	0.838
Previous ocular surgery	9 (16.1)	11 (19.6)	0.622
Systemic disease	13 (23.2)	17 (30.4)	0.393
Contact lens wear	5 (8.9)	2 (1.8)	0.438^§
Corneal lesion
Location^*			0.566
Central	34 (60.7)	31 (55.4)
Marginal	22 (39.3)	25 (44.6)
Size (mm²)			0.321
<5	34 (60.7)	39 (69.6)
≥5	22 (39.3)	17 (30.4)
Hypopyon			0.670
No	40 (71.4)	42 (75.0)
Yes	16 (28.6)	14 (25.0)
Epithelial healing time (n = 90)^†	11.1 ± 10.8	8.6 ± 9.9	0.259^Π
Surgical treatment	12 (21.4)	6 (10.7)	0.123
Initial BCVA (Snellen acuity)			0.589
<0.1	25 (44.6)	23 (41.1)
0.1-0.5	24 (42.9)	22 (39.3)
0.6-1.0	7 (12.5)	11 (19.6)
Final BCVA (Snellen acuity)			0.165
<0.1	19 (33.9)	12 (21.4)
0.1-0.5	12 (21.4)	20 (35.7)
0.6-1.0	25 (44.6)	24 (42.9)

MSS = methicillin-sensitive Staphylococcus; MRS = methicillin-resistant Staphylococcus; BCVA = best corrected visual acuity.

^* ‘Central’ is located within 1/2 radius from the center of the cornea, ‘Marginal’ is located within 1/2 radius from the limbus;

^† The eyes were excluded if surgical treatment was done (18 eyes) or the record for epithelial healing time was missed (4 eyes);

^‡ The p-value was calculated to compare the distribution between MSS and MRS by chi-square test;

^§ Fisher's exact test;

^Π independent t-test.

Table 4.

Risk factors for poor visual outcome and surgical treatment in Gram-positive bacterial keratitis (univariate logistic regression analysis)

	Poor visual outcome				Surgical treatment
Factor	No. of eyes (%)^*	OR	95% CI	p-value	No. of eyes (%)^†	OR	95% CI	p-value
	(n = 45)	OR	95% CI	p-value	(n = 22)	OR	95% CI	p-value
Sex
Female	19/69 (27.5)	1.00			10/69 (14.5)	1.00
Male	26/77 (33.8)	1.34	0.66-2.72	0.416	12/77 (15.6)	1.09	0.43-2.70	0.854
Cultured organisms				0.061				0.802
S. epidermidis	16/74 (21.6)	1.00			11/74 (14.9)	1.00
S. aureus	14/38 (36.8)	2.04	0.85-4.92	0.109	8/38 (21.1)	1.29	0.46-3.66	0.628
Strepto. spp.	11/22 (50.0)	2.96	1.05-8.39	0.041	4/22 (18.2)	1.27	0.36-4.48	0.707
Entero. spp.	7/16 (43.8)	3.62	1.11-11.86	0.033	3/16 (18.8)	1.91	0.52-7.01	0.330
Age (years)
<60	13/78 (16.7)	1.00			8/78 (10.3)	1.00
≥60	32/68 (47.1)	4.44	2.07-9.53	0.000	14/68 (20.6)	2.27	0.89-5.80	0.087
Previous ocular surface disease
No or unknown	26/101 (25.7)	1.00			12/101 (11.9)	1.00
Yes	19/45 (42.2)	2.10	1.01-4.42	0.049	10/45 (22.2)	2.12	0.84-5.35	0.112
Previous ocular surgery
No or unknown	34/119 (28.6)	1.00			15/119 (12.6)	1.00
Yes	11/27 (40.7)	1.71	0.72-4.08	0.220	7/27 (25.9)	2.43	0.88-6.71	0.087
Ocular trauma history
No or unknown	31/93 (33.3)	1.00			15/93 (16.1)	1.00
Yes	14/53 (26.4)	0.71	0.34-1.52	0.385	7/53 (13.2)	0.79	0.30-2.08	0.636
Systemic disease
No or unknown	27/104 (26.0)	1.00			14/104 (13.5)	1.00
Yes	18/42 (42.9)	2.13	1.01-4.54	0.048	8/42 (19.0)	1.51	0.59-3.93	0.395
Symptom to treatment interval
≤1 (week)	29/111 (26.1)	1.00			15/111 (13.5)	1.00
>1 (week)	16/35 (45.7)	2.38	1.08-5.24	0.031	7/35 (20.0)	1.60	0.59-4.31	0.353
Location of corneal lesion
Marginal	9/56 (20.0)	1.00			6/56 (10.7)	1.00
Central	36/90 (40.0)	3.48	1.52-7.97	0.003	16/90 (17.8)	1.80	0.66-4.92	0.251
Size of epithelial defect (mm²)
<5	12/89 (13.5)	1.00			7/89 (7.8)	1.00
≥5	33/57 (57.9)	8.82	3.95-19.72	<0.001	15/57 (26.8)	4.34	1.64-11.47	0.003
Hypopyon
No	15/105 (14.3)	1.00			4/105 (3.8)	1.00
Yes	30/41 (73.2)	16.36	6.78-39.49	<0.001	18/41 (43.9)	19.76	6.11-63.94	<0.001
Initial BCVA
≥0.1	2/78 (2.6)	1.00			1/78 (1.3)	1.00
<0.1	43/68 (63.2)	65.36	14.76-289.44	<0.001	21/68 (30.9)	34.40	4.48-264.23	0.001
Epithelial healing time (days)
<10	3/73 (4.1)	1.00
≥10	42/73 (57.5)	31.61	9.10-109.82	<0.001

OR = odds ratio; CI = confidence interval; Strepto. spp. = Streptococcus species; Entero. spp. = Enterococcus species; BCVA = best corrected visual acuity.

^* Percentage of eyes which had poor visual outcome of final best corrected visual acuity of 0.1 or less;

^† Percentage of eyes which had surgical treatment.

Table 5.

Risk factors for poor visual outcome and surgical treatment in Gram-positive bacterial keratitis (multivariate logistic regression analysis^*)

Factor	Poor visual outcome			Factor	Surgical treatment
Factor	OR	95% CI	p-value	Factor	OR	95% CI	p-value
Age ≥ 60 (years)	1.00	0.22-4.67	0.999	Age ≥ 60 (years)	0.51	0.14-1.88	0.311
Size of epithelial defect ≥5 (mm²)	3.31	0.69-15.85	0.134	Size of epithelial defect ≥ 5 (mm²)	1.35	0.41-4.43	0.617
Hypopyon (+)	4.42	0.98-19.98	0.053	Hypopyon (+)	10.96	2.66-45.18	0.001
Initial BCVA less than 0.1	36.52	6.18-215.81	<0.001	Initial BCVA less than 0.1	11.46	1.32-99.54	0.027
Cultured organism			0.528	Previous ocular surgery (+)	1.82	0.53-6.39	0.351
Strepto. spp.	2.72	0.39-18.77	0.310
Entero. spp.	5.24	0.44-62.54	0.190
Previous ocular surface disease (+)	0.82	0.21-3.21	0.785
Systemic disease (+)	0.86	0.21-3.59	0.840
Symptom to treatment interval >1 week	1.04	0.21-5.15	0.955
Central corneal lesion	0.21	0.32-1.44	0.113
Epithelial healing time ≥ 10 (days)	19.17	3.43-107.22	0.001

OR = odds ratio; CI = confidence interval; BCVA = best corrected visual acuity; Strepto. spp. = Streptococcus species; Entero. spp. = Enterococcus species.

^* Multivariate logistic regression analysis was performed for the factors which had p-value less than 0.1 in univariate logistic regression analysis.

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