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WORLD VIEW
Aetiology of suppurative corneal ulcers in Ghana and
south India, and epidemiology of fungal keratitis
A K Leck, P A Thomas, M Hagan, J Kaliamurthy, E Ackuaku, M John, M J Newman,
F S Codjoe, J A Opintan, C M Kalavathy, V Essuman,CANJesudasan, G J Johnson
.............................................................................................................................
Br J Ophthalmol
2002;86:1211–1215
Background: A multicentre study was carried out in Ghana and southern India to determine the aeti-
ology of suppurative keratitis in two regions located at similar tropical latitudes. Studies of fungal kera-
titis from the literature were reviewed.
Methods: Patients presenting at rural and urban eye units with suspected microbial keratitis were
recruited to the study. Corneal ulceration was defined as loss of corneal epithelium with clinical
evidence of infection with or without hypopyon. Microscopy and culture were performed on all corneal
specimens obtained.
Results: 1090 patients were recruited with suspected microbial keratitis between June 1999 and May
2001. Overall the principal causative micro-organisms in both regions were filamentous fungi (42%):
Fusarium
species and
Aspergillus
species were the commonest fungal isolates.
Pseudomonas
species
were most frequently isolated from cases of bacterial keratitis in Ghana but in India the commonest
bacterial isolates were streptococci
.
Conclusion: Infections of the cornea due to filamentous fungi are a frequent cause of corneal damage
in developing countries in the tropics and are difficult to treat. Microscopy is an essential tool in the
diagnosis of these infections. A knowledge of the “local” aetiology within a region is of value in the
management of suppurative keratitis in the event that microscopy cannot be performed.
S
car ring of the cornea as a result of suppurative keratitis is
an important cause of preventable blindness. In some
developing countries in the tropics, corneal infections are
the second commonest cause of blindness after unoperated
cataract.
1–3
Suppurative cor neal ulcers may be caused by
bacteria, fungi, and protozoa. However, within the tropics, as
many as two thirds of ulcers may be due to filamentous fungi.
This type of ulceration is commonly associated with ocular
trauma.
2–9
Untreated, suppurative keratitis may lead to opacification
and, ultimately, to perforation of the cornea. The associated
morbidity is the result of several factors and is directly affected
by difficulties in patient management because of a lack of
diagnostic facilities and appropriate treatment. Specific treat-
ment requires prompt and accurate identification of the
causative micro-organisms.
10
Within the setting of rural eye
hospitals in the tropics laboratory facilities are rare and diag-
nosis is based on clinical characteristics. As a direct result of
this, treatment is often empirical.
The microbial causes of suppurative keratitis vary consider-
ably between continents and countries and also within coun-
tries. It is essential to determine the local aetiology within a
given region when planning a corneal ulcer management
strategy. Several studies have investigated the epidemiology of
cor neal ulceration, causative micro-organisms, and effective
treatments, particularly in the Indian subcontinent. However
there is a paucity of infor mation in the literature with regard
to the experience in African countries.
6–8 11–14
The following study was conducted at hospitals in Ghana
and India to compare the aetiology of suppurative keratitis in
two countries, in different continents, at similar tropical
latitudes. The aims of this investigation were to improve facili-
ties for laboratory diagnosis, to determine the predominant
causative micro-organisms, to identify the most suitable
treatments, and encourage rapid referral of patients.
MATERIALS AND METHODS
Patients
A prospective study of suppurative keratitis was conducted in
Ghana and southern India between June 1999 and May 2001.
Patients were recruited at the eye unit of Korle Bu Teaching
Hospital in Accra, Ghana, and also at two rural hospitals in
Agogo (Ashanti region) and Bawku (Upper East region). In
India, patients who presented with suppurative keratitis at
two r ural “taluk” hospitals in the Tiruchirapalli district of the
souther n state of Tamil Nadu were included in the study in
addition to patients from the main study centre, Joseph Eye
Hospital (JEH) base hospital.
All patients presenting with suspected suppurative keratitis
were included in the study. Corneal ulceration was defined as
loss of corneal epithelium with underlying stromal infiltrate
and suppuration associated with signs of inflammation, with
or without hypopyon.
7
Patients with suspected or confirmed
viral keratitis were excluded from the study. Patient consent
was mandatory for inclusion in the study.
Clinical examination and laboratory investigation
Each patient was examined at the slit lamp; clinical features
were noted and a drawing made for patient records. A corneal
scrape was performed by an ophthalmologist using a sterile 21
gauge needle, or blunt Kimura spatula, following the instilla-
tion of local anaesthetic (amethocaine hydrochloride 0.5%,
without preservative). In India, lignocaine (lidocaine) 4% was
routinely administered, anaesthetic without preservative was
sometimes used. If a patient was taking antibiotics at the time
of presentation to the clinic treatment was stopped and inves-
tigations were delayed for 24 hours.
Cor neal material obtained from scraping the ulcer was
smeared onto two slides which were stained with Gram stain
and lactophenol cotton blue mountant for microscopic exam-
ination. Material was inoculated directly onto 5% sheep’s
blood agar, Sabouraud glucose agar, and into Sabouraud
broth. In India, inhibitory mould agar (IMA) was substituted
Series editors: W V Good
and S Ruit
See end of article for
authors’ affiliations
.......................
Correspondence to:
Dr Astrid K Leck,
Department of Infectious
and Tropical Diseases,
Clinical Research Unit,
London School of Hygiene
and Tropical Medicine,
Keppel Street, London
WC1E 7HT, UK;
a.leck@ucl.ac.uk
Accepted for publication
19 July 2002
.......................
1211
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for Sabouraud glucose agar, as was routine practice of the
laboratory. At the tertiary centres, if there was sufficient
cor neal material, additional culture media were inoculated
(brain heart infusion (BHI) broth, chocolate agar, and cysteine
tryptone agar). Blood agar plates, cystine tryptone agar, and
BHI broth were incubated at 37°C. Sabouraud glucose agar
plates, Sabouraud broth, and IMA plates were incubated at
27°C. A non-nutrient agar plate was inoculated if Acan-
thamoeba keratitis was suspected and an additional slide was
prepared for microscopy.
Bacteria were further identified using routine biochemical
identification tests and selectiv e media. Identification of fungi
was carried out in London and at the Mycology Reference
Laboratory, Bristol, in addition to the overseas centres. Filamen-
tous fungi were identified according to the macroscopic appear-
ance of cultures on Sabouraud glucose, potato dextrose and
cornmeal agars, and microscopic appearance of conidia and
spore bearing structures. Yeasts were identified to species level
using the germ tube test (incubation for 1.5 hours, at 37ºC, in
horse serum), Auxacolor and API kits (Bio Mérieux).
Microbial cultures w ere considered to be significant if growth
of the same organism could be demonstrated on two or more
solid phase cultures. Similarly, if there was semiconfluent
growth at the site of inoculation or growth on one solid medium
consistent with microscopy (that is, appropriate staining and
morphology with Gram stain); or semiconfluent growth at the
site of inoculation on one solid medium (if bacteria); or growth
of the same organism on repeated scraping.
171516
If, by micros-
copy, hyphae were observed in corneal tissue, but failed to grow
in culture, the causative organism was reported as fungal.
RESULTS
A total of 1090 patients presenting with suppurative keratitis
were enrolled in the study; 290 in Ghana and 800 in India. One
patient from Ghana and one patient from India presented
with bilateral infection. Fungi were identified as the dominant
causative agent of infection (including mixed infections): 44%
in southern India and 37.6% in Ghana. Bacteria were isolated
from 29.3% of cases in south India and 13.8% in Ghana (Table
1). In each case of mixed infection a single bacterial species
was associated with a single fungal species. This study
revealed a higher percentage of “mixed” infections in India
than Ghana: 5.5% versus 1.4%.
Seven patients presented with suppurative keratitis due to
infection with Acanthamoeba species in south India. The first
reported case of Acanthamoeba keratitis in Ghana was
diagnosed during this study (BJO, accepted for publication).
None of these patients were contact lens wearers.
In India 249 (31%) cases had no definitive laboratory diag-
nosis; Gram positive cocci were reported from the microscopy
in 80% (200/249) of these cases; however, cultures were nega-
tive. It was not possible to determine the aetiological agent of
144 (50%) corneal ulcer cases in Ghana (Table 1). Microscopy
and culture results were negative in 60% (87/144) of cases.
Scanty bacteria were seen in 14% (24) of Gram stained
smears. Of the remaining 33 cases which were microscopy
negative, filamentous fung i were isolated in culture from 51%
cases and bacteria from 49% cases but growth was not consid-
ered to be significant, using the criteria stated (see Materials
and methods).
Pseudomonas species were the commonest bacterial isolates
from corneal ulcers in Ghana (52.5%); P aeruginosa being the
commonest reported species. Streptococci (20%) and
staphylococci (10%) were commonly associated with corneal
infection (Table 2). In India streptococci accounted for 46.8%
Table 1 Aetiology of corneal ulcers
Type of micro-organism
India Ghana
No % No %
Definite bacterial 191 23.9 36 12.4
Definite fungal 309 38.6 105 36.2
Definite mixed 44 5.5 4 1.4
Definite
Acanthamoeba
spp 7 0.9 1 0.3
Unknown 249 31.1 144 49.7
Total 800 100 290 100
India Ghana
Microscopy and culture negative 23 87
Microscopy positive, culture negative* 218 24
Microscopy negative, culture positive 8 33
Total 249 144
*Bacteria only.
Table 2 Identification of bacteria isolated from
corneal tissue of patients with suppurative keratitis
Bacteria
India Ghana
No % No %
Gram positive cocci
Streptococcus
spp 110 46.8 8 20.0
(
Streptococcus pneumoniae
) (62) (26.4) (6) (15.0)
Staphylococcus aureus
5 2.1 2 5.0
Coagulase –ve staphylococci 58 24.7 2 5.0
Micrococcus
spp – – 1 2.5
Gram positive bacilli
Bacillus
spp 2 0.9 – –
Corynebacterium
spp – – 4 10.0
Nocardia
spp 3 1.3 – –
Gram negative bacilli
Pseudomonas
spp 35 14.9 21 52.5
(
Pseudomonas aeruginosa
) (33) (14.0)
Acinetobacter
spp 11 4.7 – –
Enterobacter
spp 3 1.3 – –
Citrobacter
spp 1 0.4 – –
Aeromonas
spp 5 2.1 – –
Klebsiella
spp 2 0.9 – –
Unidentified – – 2 5.0
Totals 235 100 40 100
Table 3 Identification of fungi isolated from corneal
tissue of patients with suppurative keratitis
Fungi
India Ghana
No % No %
Fusarium
spp 141 39.9 46 42.2
Aspergillus
spp 76 21.5 19 17.4
A flavus 59 (16.7) 9 (8.3)
A fumigatus 15 (4.2) 7 (6.4)
A niger 1 (0.3) 1 (0.9)
A nidulans – – 1 (0.9)
Aspergillus
spp
1 (0.3) 1 (0.9)
Cuvularia
spp 34 9.6 1 0.9
Lasiodiplodia theobromae
1 0.3 6 5.5
Paecilomyces
spp – – 1 0.9
Penicillium
spp 2 0.6 – –
Scedosporium apiospermum
2 0.6 2 1.8
Cephaliophora irregularis
10.3 ––
Cladosporium cladosporoides
–– 10.9
Cylindrocarpon
spp 1 0.3 – –
Exserohilum rostratum
10.3 ––
Bipolaris
spp 2 0.6 – –
Candida
spp – – 1 0.9
Unidentified 35 9.9 5 4.6
Suspected, but culture negative 57 16.1 27 24.8
Totals 353 100 109 100
1212 Leck, Thomas, Hagan, et al
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of corneal ulcers followed by staphylococci (26.8%) and
pseudomonads (14.9%). In both countries more than 80% of
bacterial isolates were represented by these three genera.
Fusarium spp and Aspergillus spp were isolated from 61% of
all fungal infections and comprised 83% of identified fungal
isolates (Table 3). Although Fusarium species were the most
prevalent fungal pathogens reported in Ghana, differences in
the spectra of fungi were observed between the participating
centres. In Accra (southern Ghana), 63% (27/43) of fungi iso-
lated were Fusarium spp compared with 31.3% (15/48) at
Bawku Hospital (northern Ghana), where a greater variety of
fungi were isolated. Lasiodiplodia theobromae was the third
commonest fungal isolate in Ghana. In India a greater
number, and diversity, of dematiaceous moulds were cultured;
Curvularia species were most frequently isolated.
DISCUSSION
Fungi were identified as the principal aetiolog ical agent of
cor neal ulceration: 44% and 37.6% of cases in India and
Ghana. Earlier studies in the same regions reported a similarly
high proportion of fungal keratitis.
612
A review of the
literature shows that there are distinct patterns of geographi-
cal variation in the aetiology of suppurative keratitis and con-
siderable variation in the proportion due to fungi has been
documented (Table 4). The proportion of corneal ulcers caused
by filamentous fungi increases towards tropical latitudes (Fig
1). In more temperate climates, fungal ulcers are uncommon
and are more frequently associated with Candida species than
filamentous fungi.
21–24
Houang et al
43
reviewed the relation of
fungal keratitis to climate concluding that, although a higher
incidence of fungal keratitis could be expected in countries
with similar annual rainfall and temperature range, this was
not always so and was also dependent on the extent of
urbanisation.
Aspergillus spp and Fusarium spp are the most frequently
reported fungal pathogens isolated from cases of fungal kera-
titis in the tropics.
5
In both Ghana and south India the most
commonly isolated fungal pathogens in the current series
Table 4 Mycotic keratitis: a review of the literature
Place Reference Year Number cases % Fungi* Organism 1 Organism 2
Europe
London Coster
17
1981 67 3% 2 cases only
London, UK Personal comm 2001 72 3%
Candida
spp 58%
Aspergillus
spp 26%
Sweden Neumann
18
1993 48 0%
North America
Florida Liesegang
19
† 1980 663 20%
Fusarium
spp 62%
Candida
spp 7.5%
Florida Rosa
20
1994 125
Fusarium
spp 62%
Candida
spp 12.5%
Philadelphia Tanure
21
2000 24
C albicans
46%
Fusarium
spp 25%
California Ormerod
22
† 1987 227 11%
C albicans
4%
Penicillium
spp 2%
Atlanta Harris
23
1988 108 32%
Candida
spp 94%
Northern USA O’Day
24
1987 33
Candida
spp 42%
Aspergillus
spp 30%
Southern USA 285
Fusarium
spp 55%
Candida
spp 9.5%
South America
Paraguay Mino de Kaspar
25
1991 26 58%
Fusarium
spp 42%
Aspergillus
spp 19%
The Middle East
Saudi Arabia Khairallah
26
1992 191 14%
Aspergillus
spp 41%
Fusarium
spp‡
Candida albicans
‡
Africa
Ghana (Accra) Hagan
6
† 1995 199 34%
Fusarium
spp 52%
Aspergillus
spp 15%
South Africa Carmichael
27
1985 274 2%
Curvularia
spp 33%
Nigeria Gugani
11
1976 59
Fusarium
spp 36%
Penicillium
spp 29%
Tanzania Mselle
28
1999 212 15%
Fusarium
spp 75%
Aspergillus
spp 19%
South Africa Ormerod
29
1987 120 2.5% 3 different isolates
Asia
Nepal, Dharan Khanal
9
† 2001 86 44%
Aspergillus
spp 60%
Fusarium
spp 13%
Nepal, Kathmandu Upadhyay
1
1991 405 17%
Aspergillus
spp 47%
Candida
spp 13%
Nepal Chaudhary
30
1999 110 8%
Rhizopus
spp 22%
Bangladesh Rahman
31
1998 63
Aspergillus
spp 35%
Fusarium
spp 35%
Bangladesh Dunlop
4
1994 66 36%
Aspergillus
spp 40%
Fusarium
spp 21%
Bangladesh Williams
32
† 1991 127 34%
Aspergillus
spp 49%
Fusarium
spp 28%
Bangladesh Williams
33
† 1987 33 21%
Aspergillus
spp 29%
Fusarium
spp 14%
India, North Chander
34
1994 730 8.4%
Aspergillus
spp 40%
Fusarium
spp 16%
India, New Delhi Panda (children)
8
1997 211 10.8%
Aspergillus
spp 40%
Fusarium
spp 11%
India, New Delhi Mahajan
35
1985 674 19.7%
Aspergillus
spp 37%
Fusarium
spp 10%
India, Mumbai Deshpande
13
† 1999 367
Aspergillus
spp 60%
Candida
spp 10%
India, Hyderabad Kunimoto
16
† 2000 102 19%
Aspergillus
spp 37%
Curvularia
spp 16%
India, Hyderabad Garg
14
2000 557
Fusarium
spp 38%
Aspergillus
spp 30%
India, Karnataka Kotigadde
36
1992 295 23%
Aspergillus
spp 34%
Candida
spp 19%
India, Madras Sudaram
37
1989 150 45%
Aspergillus
spp 53%
Fusarium
spp 12%
Penicillium
spp 12%
India, Madras Venugopal
38
† 1989 322
Aspergillus
spp 64%
Acremonium
spp 8.4%
India, Tiruchiripalli Thomas
12
1986 774 32%
Fusarium
spp 38%
Aspergillus
spp 30%
India, Madurai Rahman
39
1997 58
Fusarium
spp 38%
Aspergillus
spp 17%
India, Madurai Srinavasan
7
† 1997 434 35%
Fusarium
spp 47%
Aspergillus
spp 16%
Sri Lanka Gonawardena
40
1994 66 33%
Aspergillus
spp 18%
single isolates
Thailand Imwidthaya
41
1995 145 25%‡
Aspergillus
spp 34%
Fusarium
spp 26%
Singapore Wong
42
1997 29
Fusarium
spp 52%
A flavus
17%
Hong Kong Houang
43
2001 223 2%
Fusarium
spp 60%
*Corresponds to the proportion of fungal keratitis cases in studies which were not exclusively reporting fungal keratitis.
†Percentages of fungal keratitis cases have been recalculated by the author to represent the proportion of fungal corneal ulcers as a percentage of the
total number of corneal ulcers reported, not just those which were culture positive. Numbers of cultures can be misleading particularly if multiple isolates
are cultured from the same patient.
‡No figures stated.
Aetiology of suppurative corneal ulcers in Ghana and south India 1213
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were Fusarium spp. Other studies in south India have reported
Fusarium spp to be more common than Aspergillus species.
Fusarium spp have also been found to be the principal fungal
pathogen in Florida, Paraguay, Nigeria, Tanzania, Hong Kong,
and Singapore (Table 4). Aspergillus species predominate in
northern India, Nepal, and Bangladesh.
19133234
This phenom-
enon may be explained by differences in climate and the
natural environment. A similar pattern was also observed in
Ghana. Although Fusarium spp were the most commonly iso-
lated fungi at all of the centres in Ghana, moulds with enter-
oblastic conidia adhering in dry chains—for example Aspergil-
lus spp and Paecilomyces spp, were more frequently isolated
from patients in the north of the country where the environ-
ment is drier and dustier, than in the more humid south. As
observed by Khairallah
26
the high proportion of corneal infec-
tions caused by Aspergillus spp in drier climes may be due to
the fact that spores of Aspergillus spp can tolerate hot, dry
weather conditions. Aspergillus spp also predominate in more
temperate latitudes.
A significant increase in the number of reported cases of
suppurative keratitis was observed during the harvest period
and windy seasons. However, the proportion of corneal ulcers
due to fungi remained consistently high throughout the year.
Other authors have made similar observations, noting an
increase in cases of fungal keratitis during the dry, windy sea-
sons compared with the wet, humid months of the year.
419
This trend is likely to be a direct consequence of increased
agricultural activity before and immediately following the
rains. Some studies have reported an increase during the hot
and humid months.
835
The majority of filamentous fungi associated with corneal
ulceration in the tropics are saprobic, thermophilic moulds
that are found widely in this environment. These are
ubiquitous in the soil and vegetation. Fusarium species are
common plant pathogens, particularly of cereal crops or
saprophytes of plant debris and are found in soil.
44
The
aspergilli are ubiquitous and have been found almost
everywhere on every conceivable type of substrate, including
soil and decaying organic debris. Some of the less common
isolates such as Bipolaris spp and Exserohilum spp are
pathogens of grasses. Curvularia spp mostly occur on dead
plant material.
44
Although injury by vegetable matter is
considered to be predictive for fungal keratitis, in this study
fungal corneal ulcers were more often preceded by dust or
mud particles in the eye.
A shift in the predominant bacterial pathogens was
observed when compared with earlier findings. In Ghana,
>50% of bacterial isolates were Pseudomonas species compared
with 27% of isolates in a previous study by Hagan et al.
6
There
is a paucity of information in the literature regarding the aeti-
ology of bacterial corneal ulcers in sub-Saharan tropical Africa
and, therefore, comparisons are only possible with similar
geographical and climatic reg ions outside the continent of
Africa. Pseudomonas species were identified as the commonest
bacterial isolate in a study of 142 cases of suppurative kerati-
tis in Bangladesh in a study by Dunlop et al and also by
Williams et al, who found that 40% of bacterial isolates were
Pseudomonas spp.
433
A predominance of Pseudomonas species
has been reported in Hong Kong, Flor ida, and Paraguay.
19 25 43
In reports from Nepal and south India, Gram positive cocci
have been reported as the primary cause of bacterial
keratitis.
179
In this study, Gram positive cocci accounted for
the majority (74%) of bacterial isolates in India, as found pre-
viously by Thomas et al.
12
The proportion of bacterial ulcers
caused by Streptococcus spp increased from 18.5% (1986) to
46.8% in this study. Similar diagnostic criteria were used in
the previous study and, therefore, the trend may be
attributable to a genuine change of bacterial flora within the
geographical area, as influenced by climate and environment.
Traditional diagnostic laboratory methods, including micro-
scopy and culture may be negative despite a clear clinical
presentation of suppurative keratitis. This was true in 50% and
31% of cases in Ghana and India, respectively. This may be due
to difficulty in obtaining sufficient corneal material for
conventional investigation. This applies particularly to large,
late stage ulcers, because of the risk of perforation and,
conversely, early stage, small ulcers from which little material
is available. It is imperative that the quality and quantity of
specimen is optimal for accurate laboratory diagnosis. Self
administration of antibiotics by patients before seeking medi-
cal attention has been thought to affect the recovery of organ-
isms in culture.
4
It is possible culture positivity correlated with
inappropriate antibiotic usage.
Although there were a high proportion of corneal ulcers in
Ghana for which the aetiology was not determined, the
number of proved fungal ulcers at each of the centres was
greater than the number of proved bacterial ulcers. It is there-
fore not unreasonable to assume that this trend could be
extrapolated.
It is usually not possible to determine the significance of
bacteria observed by microscopy alone. Small numbers of
Gram positive cocci may be contaminants from the lid margin.
Conversely, the presence of fungal hyphae in corneal tissue is
significant. In agreement with Dunlop et al the sensitivity, spe-
cificity, and predictive value of Gram stain microscopy is much
higher for fungal ulcers than those caused by bacteria.
4
In this
study 95% of fungal infections could have been diagnosed
based on the findings from microscopy alone. This is an
important conclusion, since the majority of rural based clinics
in areas where suppurative keratitis is a problem do not have
culture facilities but m ay be able to perform simple
microscopy. A wet mount preparation, using lactophenol cot-
ton blue stain, was used as a supplementary stain in this
Figure 1 Suppurative keratitis due
to fungi as a proportion of total
number of cases, by latitude.
1214 Leck, Thomas, Hagan, et al
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study. Where scientific expertise, and/or resources, may be an
issue, it is easier to observe fungal hyphae employing this
method than using the potassium hydroxide (KOH) tech-
nique. Reports into the presence of fungi in the eyes of
asymptomatic individuals, have shown that a wide variety of
fungi may be transient in the conjunctival sac. This may be the
case in as many as 37% of healthy eyes, thereby discounting
the use of single culture.
11
In conclusion, it is imperative to know the “local” aetiology
of keratitis in a particular region. Our comparative study dem-
onstrates that there were differences between two countries
with similar tropical climates at the same latitude. Equally,
differences were observed within the same country. This is
important information with regard to management, as many
eye units do not have microscopy or culture facilities. Diagno-
sis is then dependent on clinical acumen and the treatment
provided is, at best, empirical. It is clear that it is important to
know the local aetiology, particularly if diagnosis is going to be
reliant on clinical signs alone. Changing patterns of disease
have also occurred in temperate, developed countries, as
exemplified by the increase in keratitis due to Pseudomonas spp
and Acanthamoeba spp in recent years. Awareness of changes in
aetiology and antimicrobial resistance, when this information
is available, are critical to managing keratitis cases.
ACKNOWLEDGEMENTS
The authors would like to thank the staff of Korle Bu, Bawku, and
Agogo hospitals (Ghana) and Musir i, Ariyalur, and Myladthurai hos-
pitals (India) for their assistance during this study. Also, Miss Linda
Ficker, Dr Allen Foster, and Dr Elizabeth Wright for their clinical
guidance.
.....................
Authors’ affiliations
A K Leck, G J Johnson, Department of Infectious and Tropical Diseases,
Clinical Research Unit, London School of Hygiene and Tropical Medicine,
Keppel Street, London WC1E 7HT, UK
P A Thomas, J Kaliamurthy, M John, C M Kalvathy, C A N
Jesudasan, Institute of Ophthalmology, TELC-Joseph Eye Hospital,
Tiruchirapalli, South India
M Hagan, E Ackuaku, M J Newman, F S Codjoe, J A Opintan, V
Essuman, Korle Bu Teaching Hospital, Accra, Ghana
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2002 86: 1211-1215Br J Ophthalmol
A K Leck, P A Thomas, M Hagan, et al.
fungal keratitis
Ghana and south India, and epidemiology of
Aetiology of suppurative corneal ulcers in
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