Evaluating the diagnosis and management of oculomycosis in Ghana

Article history: Received on: 23/08/2016 Revised on: 04/09/2016 Accepted on: 30/10/2016 Available online: 29/11/2016 Appropriate diagnosis and treatment of oculomycosis is crucial in curbing its associated visual impairment. This study therefore evaluated the diagnosis and management of oculomycosis in Ghana. A cross-sectional survey involving 120 eye care practitioners from six regions of Ghana was conducted. Using a structured questionnaire, information on procedures of diagnosis and management of oculomycosis were collected. Clinical features were considered by 66.7% eye care practitioners in diagnosing oculomycosis, with only 37.5% requesting for laboratory investigations. Fluconazole (79%) and natamycin (44%) were the most commonly prescribed antifungal eye drops by practitioners based on efficacy. Majority of practitioners (59.2%) reported non availability of antifungal eye drops from pharmacies. Age, profession, location of facility and type of facility were strongly associated (P ≤ 0.01-0.001) with the practitioners’ diagnostic practice of requesting for laboratory investigations. Diagnosis of oculomycosis in Ghana is based more on clinical features, especially in the district areas, than on microbiological investigations, which does not augur well for better prognosis and management. Treatment is mainly by systemic antifungals, as antifungal eye drops are hard to come by. While a successful therapy was not without some visual consequences, it reduced significantly corneal scarring, blurred vision, and blindness associated with oculomycosis.


INTRODUCTION
Oculomycosis is gradually becoming a public health issue as it remains one of the most difficult and challenging ocular diseases to diagnose and treat by eye care practitioners (El-Seidi et al., 2006).Prompt diagnosis and treatment of oculomycosis is imperative to prevent vision-threatening complications of the infection.Clinical signs and features, such as the formation of hyphae in the cornea (Rajmane et al., 2011), an indolent course, irregular feathery margins, dry texture, corneal satellite lesions, hypopyon, corneal ulcer, and keratitis are suggestive of oculomycosis (Graff et al., 2006).Clinical symptoms include photophobia, chemosis, redness, tearing and severe ocular pains (Nayanar and Vanathi, 2012).Using clinical features alone to diagnose oculomycosis is sometimes not reliable as it cannot distinguish it from other microbial infections These regions were chosen based on the number of practitioners and distribution of eye care facilities to ensure appropriate representation of participants across the country (National Eye Care Report, 2005).

Study population
The study population comprised three categories of eye care practitioners: Ophthalmologist, Optometrist and Ophthalmic nurses.These practitioners were selected because they were deemed to have knowledge in ocular disorders including oculomycosis.An ophthalmologist is a specialist in medical and surgical eye problems.An optometrist is the first point of call in case of eye conditions, therefore has gained the expertise to diagnose and treat simple ocular disorders of common occurrence, while an ophthalmic nurse is also trained to work with other eye care professionals in managing ocular disorders.

Eye care facilities involved in this study
Teaching hospitals, Government hospital (GHS), Christian Health Association of Ghana (CHAG) hospitals, as well as private and Non-Governmental Organizations (NGOs) comprised the selected hospitals and eye clinics from the regions used.The different health facilities influence the number of patients visiting, as well as the kind of cases reported to the facility, and hence the diagnosis and management of a disease/disorder.

Sampling size
A total of 120 eye care practitioners were recruited from the various eye care facilities.The sample size was deemed appropriate based on information obtained from the Eye Care Unit Annual Report 2011, and from calculation based on Glenn's equation, i.e.N o =z 2 pq/e 2 [Where N 0 is Sample size, z 2 is the abscissa of the normal curve that cuts off an area  at the tails (1- equals the desired confidence level, e.g.95%), e is the desired level of precision, p is the estimated proportion of an attribute that is present in the population and q equals to 1-p].

Sampling technique
Cluster sampling was used in recruiting participants.First and foremost, each eye care facility in a specific region was classified based on its location as rural (those located in districts areas) or urban (those located in metropolitan areas).For each region, two rural and three urban eye care facilities were then randomly selected to participate in the study.Ophthalmologists were recruited firstly, followed by Optometrists and then Ophthalmic nurses during a visit to selected facilities.This order format followed the ranks and the expertise in terms of handling cases related to the eye.

Study design and instrument for data collection
A cross-sectional survey of optometrist, ophthalmologist and ophthalmic nurses was conducted using structured questionnaire designed to cover the following: Bio-data of eye care practitioner's practices regarding diagnosis, request for microbiological investigations, and antifungal therapy selection among others.Questionnaires were self-administered by the practitioners within a time frame of 5 minutes.An initial testing of the questionnaires was carried out using 10 practitioners to assess the ability of this study instrument in obtaining data suitable for this study.

Inclusion criteria
For a professional to be included in this survey, that individual should be a registered eye care practitioner in active practice, being involved in diagnosing and managing of ocular diseases and disorders including oculomycosis, and having had at least one year working experience after their internship were eligible for the study.Practitioners who were registered but not in active service or had less than a year of working experience, as well as those that had retired from active service were excluded from the study.

Limitations to the Study
The data collection method used may not have allowed practitioners enough time to come out with more information like an in-depth interview could have provided.The study assumed that the responses given by participants were representative of what happens in the eye care facilities in Ghana.Hawthorne's effect could also have affected the responses of some practitioners since they knew it was a study and could present information that was actually not the case.

Ethical consideration
The study was approved by the Department of Pharmacology, KNUST, ethics committee.Informed consent was obtained from all practitioners before participation in accordance with the tenets of Declaration of Helsinki regarding the use of human subjects for research.In addition, permission was obtained from the Head of each health facility used for the study.Responses by participants were kept confidential by not taking their names.Participants were not given any incentives or influenced in any way to part-taking in the study, and had the freedom to opt out of the study at will.

Data analysis
Data obtained was collated and analyzed using SPSS V 20 (SPSS, Chicago, Illinois, USA).Pearson's chi-square ( 2 ) was used to show relationship between two categorical variables.P  0.05 was considered significant.Sigma Plot V 11 (Systat Software, Inc., San Jose, CA) was used to plot the graphs.

Demographics of practitioners
Out of 120 practitioners who participated in this survey, 63 (52.5%) were males and 57 (47.5%) were females.Fifty-two (43.3%) were Optometrists, 51 (42.5%)Ophthalmic nurses, and 17 (14.2%)Ophthalmologists.The majority of these practitioners 40.0%(48) were aged 21-30 years with only 16 (13.3%)aged 50 years or older.Majority, 68 (56.7%) had worked for at most 3 years with 12 (10.0%)having worked for over 13 years (Table 1).Sixty-two (51.7%) of the practitioners worked in health facilities located in the District, while 58 (48.3%) worked in eye clinics located in the Metropolis.The practitioners were almost equally distributed across the different types of eye care facilities in the country (Table 2).

Factors considered in diagnosis of oculomycosis
Practitioners who considered: history of presenting complain were 80 (66.7%); findings of slit-lamp biomicroscopy were 96 (80%), and unresolved corneal ulcer to conventional antibiotic treatment were 47 (39.2%) (Figure 1).Clinical signs, symptoms and features seen on examination with slit lamp biomicroscopy that aided diagnosis of oculomycosis were reduce visual acuity, cornea ulcer, keratitis, and hypopyon among others (Figure 2).

Diagnosis by laboratory investigation
Only few practitioners, 45 (37.5%) requested for microbial laboratory investigation to establish a fungal involvement in a suspected case of oculomycosis.Of these, 31 (68.9%)requested for corneal scraping and culturing.Twenty-four 24 (20%) requested for microbiological investigations either when there was unsuccessful treatment with conventional antibiotics, while 32 (26.6%) requested when there was characteristic fungal corneal ulcer appearance.

Factors associated with practitioner's request on laboratory investigation
Age of practitioners (P ≤ 0.001), type of profession (P = 0.003), location of facility (P = 0.008), and type of facility (P ≤ 0.001) were factors significantly associated with the request or otherwise for laboratory investigation for fungal isolation leading to the diagnosis of oculomycosis.A greater proportion of females, 24 (53.3%),requested for laboratory investigations (Figure 3); although the association between gender and request for laboratory investigations was not significant (P = 0.350).The majority of practitioners age between 41-60 years were those requesting for laboratory investigations in situations of suspected oculomycosis (Figure 4).The majority of Ophthalmologists, 10 (58.8%), did request for laboratory investigation for the diagnosis of oculomycosis, unlike the other two eye care professionals (Figure 5).

Fig. 5:
The association between the professional and laboratory investigations request.There was significant difference (P = 0.003) between kind of eye care practitioner and their request for laboratory investigations on oculomycosis.(Pearson's Chi Square ( 2 ) test) Also, an equal number of the practitioners who had practiced between 9-13 years did request for laboratory investigation to aid in diagnosis of oculomycosis, as compared to the others.There was no significant difference (P = 0.564) between the duration of practice of the eye care practitioners and their request for laboratory investigation on oculomycosis (Figure 6).

Fig. 7:
The association between location of facility and request for laboratory investigation.There was a significant difference (P = 0.008) between the location of eye facilities of eye care practitioners and their request for laboratory investigations (Pearson's Chi Square ( 2 ) test).
While an equal number of practitioners 33 (27.6 %) located in the metropolis request for laboratory investigation towards the diagnosis of oculomycosis, majority of those located in the districts do not (Figure 7); thus location of practice (i.e.metropolitan or district) was associated (P = 0.008) with the request for laboratory investigation on oculomycosis.Most of the practitioners working with teaching hospitals, 21 (70%), requested for laboratory investigations, as compared to those in other facilities (Figure 8).

Topical ocular antifungal agents and its accessibility
Out of the total number of practitioners who undertook this study, 71 (59.2%) reported difficulties in accessing topical ocular antifungals and 80 (66.7%) reported that their patients, even if they did, obtained their prescription from retail pharmacies instead of hospital pharmacies.The common topical ocular antifungals that practitioners prescribed were fluconazole (79%), natamycin (44%), extemporaneously prepared miconazole (31%) or econazole eye drops (7%).According to the practitioners, these drugs were selected due to their efficacy.

DISCUSSION
Proper diagnosis of any disease or disorder helps in rapid, accurate and proper selection of drugs, as well as in proper treatment; to improve the chances of a complete recovery (good prognosis).This study therefore evaluated diagnosis and management practices of oculomycosis in Ghana.In this study, characteristic clinical symptoms of oculomycosis were used by the majority of eye care practitioners, and these were based on the history of presenting complain (HPC), clinical examination (using slit lamp biomicroscopy), and unresolved corneal ulcer to conventional antibiotic treatment; these modes of diagnosis for oculomycosis have also been reported widely (Jastaneiah et al., 2001, Ansari et al., 2013, Thomas, 2003and Mravičić et al., 2012).The details elicited in HPC included trauma with vegetative matter, sand, soil, stone, spontaneous occurrence, use of herbal and other unknown eye drops.Trauma occurs from ocular injuries (sometimes trivial) involving some type of vegetable matter, soil and sand related to the physical activities of people.Trauma has been reported by Srinivasan et al., 1997 to be the most common predisposing factor of oculomycosis.Oculomycosis could occur without any known cause as some patients' report, but it could be that particular attention was not paid to the predisposing factor.Some characteristic clinical features informing a diagnosis of oculomycosis (using a slit lamp biomicroscopy) as reported by some eye care practitioners were corneal ulcer, keratitis (i.e. a corneal inflammation characterized by cornea haziness, superficial punctate stains, and oedema, and even in some cases corneal bullae), indistinct cornea margins, stromal infiltrates, satellite lesions, cornea degenerations (rough texture, raised borders, brown pigmentations), endothelial plaques, and other corneal features.These are specific clinical features of oculomycosis (Thomas, 2003;Mravičić et al., 2012).Non-specific features such as hypopyon, discharge, injections or redness, and fluorescein stain pattern (hyphae like pattern) were also reported.
Within the setting of rural eye hospitals in the tropics, laboratory facilities are rare and diagnosis is based on clinical characteristics.As a direct result of this presumptive diagnosis, treatment is often empirical (Leck et al., 2002).
Microbiological investigations are essential for identification of fungus to confirm diagnosis of suspected oculomycosis.From our study, forty-five practitioners requested for microbiological investigations, only after there was unsuccessful treatment with conventional antibiotics or when there was characteristic fungal corneal ulcer appearance.This practice of diagnosis is essential but cannot be relied on alone in recent years.It has been suggested that where facilities are available, microbial investigation is the most important practice to help in diagnosis and prevent delays which can cause visual impairments.Ansari et al., 2013, reported that because of overlapping clinical features of the etiologic agents of keratitis which makes it difficult to distinguish one from another, tissue sampling and culture continues to be an imperative utility in the diagnosis of oculomycosis.
Practitioners indicated that samples were collected by corneal scraping for culture and sensitivity test.Corneal scraping and culturing procedures are very important for the isolation of fungi (Ansari et al., 2013).Fungi can penetrate deeper layers of the cornea, so tissue swabbing is inadequate in isolating or confirming fungal agent involved in oculomycosis.Corneal scraping using a surgical blade is recommended to obtain a tissue specimen (Ansari et al., 2013).
Although in clinical practice, females request for microbiological investigations more than males, and that females are more meticulous with a step to step approach in clinical examination before making diagnosis, there was no significant association to that effect as far as this study was concerned.This augurs well for the practitioners practice in Ghana as one should not be of a particular gender in other to request for microbial investigation.It was observed from the results of this study that, the more one gets older in practice, the more likely they would request for microbiological investigation for suspected oculomycosis.Majority of ophthalmologists were older professionals, and requested for microbiological investigation, unlike the other eye care professionals.In an earlier study (Gyanfosu et al., 2016), findings indicated that Ophthalmologists encountered more ocular disorders than the other eye care professionals, hence making them more proficient in the diagnosis and management of oculomycosis (Dahl et al., 2014).Ophthalmologists receive special training in all aspects of eye care, including prevention, diagnosis, and medical and surgical treatment of eye conditions and diseases, thus providing the full spectrum of eye care.Optometrists provide primary eye care services, including eye examinations and diagnosis of eye diseases taking intermediate (6-7yrs) length of training.It is worth noting that although each professional's responsibilities differ, and depending on the setting of the health facilities, there are overlapping job description.
It was also found that health facilities located in the Metropolitan areas showed borderline association to the request for microbiological investigation for oculomycosis; implying that a significant number of practitioner in the metropolitan areas make the request.This could be influenced by the availability of many medical laboratories in the cities compared to the districts.
The practitioners indicated the common fungi isolated were Aspergillus spp, Fusarium spp and Candida albicans.Our study revealed Candida albicans to be the most common fungi isolated during microbiological investigation.In 1995, Hagan et al., found Fusarium spp to be the common fungi followed by Aspergillus spp to be the cause of suppurative keratitis in Ghana.Other studies have also mentioned many different fungal species isolates (Thomas et al., 2013, Jastaneiah et al., 2001, Ibrahim et al., 2012, Leck et al., 2002, Hagan et al., 1995).Candida albicans are part of the normal eye flora which reside as a lifelong, harmless commensal.It is not surprising that Candida albicans is the most common fungi isolate, because it has been shown to have a high virulence in ocular infections (Schreiber et al., 2003).
Oculomycosis, if not diagnosed and treated with celerity, can be rapidly destructive to the integrity of the eye, resulting in devastating ocular damage.The main aim of treating oculomycosis is to preserve vision which depends on rapid diagnosis and efficient administration of appropriate antifungal therapy.Access to topical antifungals is generally difficult in Ghana as reported by the eye care practitioners.Worldwide, access to commercially available topical antifungals is also low (Ibrahim et al., 2012).Majority of the practitioners indicated that patients obtained topical antifungal medications from retail pharmacies instead of hospital pharmacy.Ocular topical antifungals are not on the NHIS medicines list (http://www.nhis.gov.gh/MedList.aspx).Most hospitals stock their pharmacies based on their prescriptions which is also based on the essential medicine list (EML, 2010) and the NHIS drug list.Even though ocular antifungal eye drops are on the essential medicine list, but because they are not on the NHIS listed medicines, hospitals do not stock them.Retail pharmacies usually buy and stock varieties of medicines from pharmacy wholesalers, and hence patients acquire these medications from them.
The practitioners admitted that fluconazole is the common topical antifungal readily available in Ghana.The eye care practitioners reported that extemporaneous preparation made from gyno-daktarin (which contains miconazole) cream was used as antifungal eye drops for patients when access to standard topical antifungals was difficult.The various topical antifungal preparations selected were effective and accessible as reported by the eye care practitioners.Oculomycosis presents a visual impairment to the patient if the condition is not diagnosed early for a rapid and appropriate intervention.Some prominent adverse effects after treatment of oculomycosis as reported by eye care practitioners were corneal scarring, blurred vision, redness of the eye, reduced vision, and blindness.

CONCLUSION
Diagnosis of oculomycosis is based more on clinical features, especially in the district areas, than on microbiological investigations, which does not augur well for better prognosis and management.Treatment is mainly by systemic antifungals, as antifungal eye drops are hard to come by.While a successful therapy was not without some visual consequence, it significantly reduced corneal scarring, blurred vision, and blindness associated with oculomycosis.Avenues to obtaining topical ocular antifungals should be created, while efforts to include some of these topical antifungals in the NHIS medicine list should be initiated.This then will enhance diagnosis and ensure effective management of oculomycosis, and increase the chances of complete recovery.

Fig. 1 :
Fig. 1: The mode of diagnosis of oculomycosis employed by the eye care practitioners.SLE= Slit lamp Examination; DCAT= Difficulty with conventional antibiotic treatment.

Table 1 :
Age and duration of practice of 120 eye care practitioners

Table 2 :
Location of practice for practitioners interviewed Distribution Frequency