Description of the sample
Table 1 presents the sociodemographic, socioeconomic and healthcare status characteristics of the study participants. Out of the 114 patients presenting with external ocular and periocular infections, majority were females (56.1%), of median age of 17.0 (Interquartile range; 29.75) years (Table 1). The majority of the participants were aged 3-17 years (29.8%), of Akan tribe ethnicity (93.0%), and with a protestant religion (80.7%). Most of them lived in a rural community (59.6%), with their highest education level being primary (33.6%) and major occupation as students (43.9%). An equal proportion were single (21.2%) and married (21.2%) and the remaining either cohabiting (3.5%), divorced (2.7%), widow (1.8%) or separated (0.9%). A preponderance of participants never smoked (52.6%), and with a significantly higher average alcohol intake in males compared to females (p = 0.027). Approximately 6% had hypertension and an equal proportion had diabetes (4.4%) and peptic ulcer (4.4%). The number of patients on antihypertensive, antidiabetic and antibiotic medications were 5.3%, 3.5% and 3.5%, respectively.
Clinical characteristics of external ocular and periocular infections among study participants
Table 2 shows the clinical characteristics of external ocular and periocular infections among study participants. Most presented with both eyes infected (66.7%) with the conjunctiva (94.7%) as the commonest affected site. The majority of the participants had previously used antimicrobials (55.8%) and have had previous eye infections (45.1%), and with duration of infection less than one-week (63.7%). There was a variation between males and females in terms of previous ocular trauma (p = 0.023) and previous use of mascara (p = 0.015). With respect to monocular visual acuity, majority had right eye visual acuity better than 6/18 (63.8%) and with a fewer having visual acuity worse than 6/60 (2.6%). Most had a left visual acuity within the ranges 6/5-6/6 (67.5%) and fewer proportion (1.8%) having visual acuity better than 6/60 but worse than 6/24. The commonest presenting symptom was hyperemia/redness (69.3%), followed by discharge, (62.3%) itching (60.5%), eye pain (50.9%) and a smaller fraction having falling lashes (0.9%). Majority received a minimum of two antibiotics for treatment of infections (40.4%) and with a fewer portion (7.9%) having other treatment other than antibiotics. The proportion of clinical presentations were conjunctivitis (60.5%), keratoconjunctivitis (11.4%), blepharoconjunctivis (9.6%), keratitis (7.9%), ocular trauma (6.1%), hordeolum (2.6%), Preseptal cellulitis (0.9%) and ophthalmia neonatorum (0.9%). Other associated conditions were dry eyes (10.5%), headaches (5.3%), pterygium (4.4%) and pinguecula (0.9%). The commonly used antimicrobial therapeutics were polymyxin B (41.2%), neomycin (35.1%) and ciprofloxacin (31.6%) and fewer instances gentamycin (2.6%) and ofloxacin (1.6%) as shown in Table 3.
Bacteria etiology of external ocular and periocular infections among study participants
One hundred and three (103) ocular specimens were enrolled for bacteriological investigation, 98 (95.1%) were culture positive, no mixed cultured was identified (Please see Table 3). The proportion of Gram-negative bacteria was 58.2% with Pseudomonas aeruginosa (38.8%) and Pseudomonas putida (11.2%) being the predominant species. Conversely, the prevalence of Gram-positive bacteria was 41.8%, with a preponderance of bacteria pathogens being Staphylococcus aureus (27.6%) and Coagulase negative staphylococci, CONS (13.3%). The commonest strains of bacteria pathogens isolated from conjunctivitis were Pseudomonas aeruginosa (40.0%), Staphylococcus aureus (21.8%) and Pseudomonas putida (16.4%). Similarly, Pseudomonas aeruginosa (41.7%) and Staphylococcus aureus (33.3%) were frequently identified in cases of keratoconjunctivitis. Staphylococcus aureus (100.0%) was the sole organism implicated in cases of preseptal cellulitis, whereas most cases of keratitis was caused by Pseudomonas aeruginosa (75.0%) as shown in Table 4.
Factors associated with external ocular and periocular infections
Table 5. shows logistic regression analyses of the association between patients’ demographics, clinical characteristics and prevalence of bacterial infection. None of the factors was significantly associated with prevalence of bacterial infections (p > 0.05).
The novel study for the first time aims to investigate the bacteria etiology of external ocular and periocular infections and antimicrobial treatment patterns among a Ghanaian ophthalmic population. About 95% of the culture were positive for bacteria pathogens, and with the predominant class of bacteria being Gram negatives. Pseudomonas aeruginosa and Staphylococcus aureus were the commonly isolated bacteria species and with the former frequently isolated in cases of conjunctivitis and keratitis. The commonly used antimicrobial therapy in the clinical management of eye infections in these facilities were polymyxin B, neomycin and ciprofloxacin.
Bacteria ocular and periocular infections pose health challenges owing to associated morbidity and blindness. Globally, the burden of bacteria eye infections is higher especially in lower-and-middle income countries including Ghana2-4. Though microscopic, the wide biodiversity of bacteria pathogens makes it burdensome for ophthalmic clinicians and physicians when selecting appropriate antibiotic therapy in routine clinical management of ocular and periocular infections. Previously, authors from several geographical jurisdictions have investigated the burden and etiology of bacteria eye infections, however, outcomes from these studies varied considerably 13-15,18,20,25,26. The prevalence estimates of medical conditions such as bacteria ocular and periocular infections are critical in informing eye care service delivery and in the development of policies to strengthen eye care practices yet there is presently limited ophthalmic data to propagate such transitions within the Ghanaian context. Importantly, gaining insight on bacteria etiology implicated in cases of external ocular and periocular infections within the Ghanaian population is essential to guide clinicians in the appropriate choice of antimicrobial therapy. Nonetheless there is paucity of data in this regard.
Overall, the prevalence of bacteria ocular and periocular infections found in this study was 95.1%. Our results are comparable with studies in Ethiopia 50, Saudi Arabia 51, Italy 25 and United states of America26. In a cross-sectional study in Ethiopia, Tesfaye et al. reported a prevalence of 74% 50. Similarly, a study by Shahaby and colleagues utilizing participants from a university clinic in Saudi-Arabia found more than two thirds of ocular specimens harboring bacteria pathogens 51. Likewise, an observational case series conducted in Italy by Papa and coworkers, revealed that the proportion of bacterial infections was estimated at 72.5% 25. Furthermore, in a prospective observational study among patients undergoing cataract surgery in the USA, Ta et al. showed that almost eight of every ten ocular specimen obtained from patients eyes had a bacteria etiology 26. On the one hand, estimates from the present study is significantly higher and varies substantially compared to studies in China 13,18, Iran 20, South Korea 14 and Nepal 15 with prevalence estimates far lower than 50% 13-15,18,20. Although geographical settings, study population, seasonality and laboratory procedures could account for such variations as reported earlier, a plausible reason for our observation may be attributable to the fact that our study unlike previous investigations enrolled patients from multiple eye care facilities hence the burden of infections maybe summative. Another reason is that majority of our study participants were rural dwellers with sanitation in such areas usually problematic compared to inhabitants in urban vicinities.
We observed a slightly higher proportion of Gram-negative bacteria compared to Gram positives as etiological agent in our study. This findings contrast with studies from China 13, Ethiopia 11, Saudi-Arabia 16, Uganda 4 and United States of America 26 where Gram negatives were found to be significantly lower compared to Gram positive bacteria and with proportional estimates of ranging from six to ten percent 4,11,13,16,26. Conversely, the proportionate distribution of Gram negatives to positive bacteria found in this study are parallel with results from several existing literatures 2,5,8,10. For example, among the various ocular microbiology investigations conducted across Ethiopia, by Ayebubizu et al. 5, Belyhun et al.2, Assefa et al.10 as well as Getahun and colleagues 8 the proportionate distribution of Gram-negatives were similar to Gram positives. Of note, whereas the magnitude of Gram-negative bacteria etiology found in Australia 21, Iran 20 and Italy 24 were not equivalent to our findings as well as studies in parts of Ethiopia, the proportion estimates reported were relatively higher. There exist regional variations in the patterns of distribution of Gram-negative bacteria, however, the higher prevalence in our study are ascribed to hygiene as the primary mode of transmission of these enteric bacteria are through oral-fecal contamination. Specifically, we observed during data collection that most patients repeatedly clean ocular discharges with either bare hands or face handkerchief, hence predisposes eyes to contamination by fecal contaminants. Additionally, majority of our study subjects were either in preschool and/or primary hence prone to eye contamination through outdoor gaming activities in school. A considerably higher proportion of the study participants were below two years, and these age categories frequently experience oral-ocular contamination through inserting hands in mouth and touching of eyes thereafter which may have accounted for the increasingly abundance of Gram negative bacteria than positives in our study.
The predominant bacteria species found in our study were Pseudomonas aeruginosa and Staphylococcus aureus. Although, S. aureus was second only to P. aeruginosa as the frequently isolated bacteria pathogen, however, it remains the most abundant Gram positive bacteria isolate from all obtainable ocular specimen in our study. This finding are consistent with studies in India 19, Italy 24, Nigeria 52, and Ethiopia 4,8,12. The occurrence of ocular infections with S. aureus etiology may be due to frequent touching of eyes with filthy hands among study subjects. The incidence of Pseudomonas aeruginosa in eye infections are mostly linked with the wearing of contact lens nonetheless we observed an inverse trend in our study. The blinding risk factor associated with Pseudomonas aeruginosa ocular infections underscores the promotion of contact lenses as an alternative to spectacle glasses in vision correction and/or cosmesis. Importantly Pseudomonas aeruginosa are opportunistic pathogens with devastating consequences on the ocular tissues. Specifically, they induce cornea infiltration and ulcerative keratitis when improperly managed by clinicians. Further, the conjunctiva and cornea are in close proximity landmarked by the limbus, hence pathogens of the conjunctiva can easily spread to the cornea during physiological blinking or mechanical rubbing of the eyes. Given the predominance of Pseudomonas aeruginosa in cases of conjunctivitis and keratitis warrants the need for clinicians to probe for other proxy predisposing factors other than relying solely on contact lenses etiology in most instances.
The commonly administered antimicrobial therapy found in this study were Polymyxin B, neomycin and ciprofloxacin. Polymyxin B is a nonribosomal peptidic antimicrobial agents used mostly in the treatment of Gram-negative infections. In particular, they exert their bactericidal effect by binding to phosphate residues within the lipopolysaccharides cell wall to induce displacement of divalent magnesium and calcium cations known to maintain membrane stabilizing properties of Gram-negative bacteria. Consequently, the intrinsic mechanism of action primarily causes an increase in cell membrane permeability resulting in a direct loss of cytoplasmic cell contents. Furthermore, they act synergistically with beta-lactam antibiotics by exposing the peptidoglycan machinery of these Gram negatives for which the latter act on 53. On the contrary as an aminoglycoside neomycin actively inhibits protein synthesis of bacteria by insurmountably binding to the 16S ribosomal RNA as well as 50S ribosomal subunits of susceptible class of Gram bacteria 54,55 . Similarly, ciprofloxacin a fluoroquinolone prevents bacteria DNA replication by terminating the action of the reaction enzymes DNA topoimerase IV and DNA gyrase. The ensued effect is suicidal against Gram negatives as well as mixed bacteria culture 56. Altogether, the frequent use of the aforementioned antibiotic agents in clinical management of ocular and periocular eye infections in our study are concordant with the laboratory results which identified Gram negatives as the predominant bacteria isolates.
Of note, the study has several strengths worth highlighting. The study presents a preliminary and most recent data on bacterial etiology of external ocular and periocular infections among ophthalmic patients in Ghana. Although, we recommend future ocular antibiotic sensitivity studies in this setting, however, in light of the present evidence on the bacterial isolates implicated in eye infection are essential in assisting ophthalmic clinicians in their choice of antibiotic therapy. Moreover, unlike previous studies2,7,57 the present investigation utilized sample from multiple sites which underscores the selection bias usually associated with the convenience sampling approach which the study employed. On the contrary, owing to resource limitation the study could not performed direct fluorescent antibody test and/or Giemsa staining to investigate infections of Chlamydia trachomatis etiology. Our prevalence may have been underestimated as a considerable number of our patients where preschoolers whose uncooperative nature denied researchers from taking ocular swabs for bacteriological analyses.