Clinical Characteristics of External Ocular and Periocular Infections and Their Antimicrobial Treatment Patterns Among a Ghanaian Ophthalmic Population; A Multicenter Study

Isaiah Osei Duah Junior Department of Optometry and Visual Science, College of Science, Kwame Nkrumah University of Science and Technology, Kumasi Michel Pascal Tchiakpe Department of Optometry and Visual Science, College of Science, Kwame Nkrumah University of Science and Technology, Kumasi Lawrence Sheringham Borquaye Department of Optometry and Visual Science, College of Science, Kwame Nkrumah University of Science and Technology, Kumasi Kwadwo Amoah The Eye Clinic, Kumasi South Hospital, Atonsu-Agogo, Kumasi Francis Kwaku Dzideh Amankwah Department of Pharmaceutics, Faculty of Pharmacy and Pharmaceutical Sciences, Kwame Nkrumah University of Science and Technology, Kumasi David Ben Kumah Department of Optometry and Visual Science, College of Science, Kwame Nkrumah University of Science and Technology, Kumasi Linda Aurelia Ofori Department of Theoretical and Applied Biology, College of Science, Kwame Nkrumah University of Science and Technology, Kumasi Anthony Danso-Appiah Department of Epidemiology and Disease Control, School of Public Health, University of Ghana, Legon Bright Owusu Prempeh The Anglican Eye Hospital, Jachie Stephen Yao Gbedema Department of Pharmaceutics, Faculty of Pharmacy and Pharmaceutical Sciences, Kwame Nkrumah University of Science and Technology, Kumasi Justin Munyaneza Department of Optometry and Visual Science, College of Science, Kwame Nkrumah University of Science and Technology, Kumasi Cynthia Amaning Danquah Department of Pharmacology, Faculty of Pharmacy and Pharmaceutical Sciences, Kwame Nkrumah University of Science and Technology, Kumasi Kwadwo Owusu Akuffo (  koakuffo@gmail.com ) Department of Optometry and Visual Science, College of Science, Kwame Nkrumah University of Science and Technology, Kumasi

These infections are usually treated with antimicrobial agents with varying modes of action. The gold standard treatment for ocular infections starts with culture and sensitivity testing to identify the causative organism and subsequent administration of narrow-spectrum antibiotic therapy 31 . Consequently, as a results of resource limitation and unavailability of testing facilities most clinicians; including eye care professionals engage in empirical treatments with broad-spectrum antimicrobials 32 . The irrational and prolonged use of broad-spectrum antibiotics in treating eye infections could alter the genetic makeup of ocular bacteria and consequently lead to to antimicrobial resistance 33 .
Ocular antimicrobial resistance is a growing public health threat in both advanced and developing countries. In the developed world nationwide surveillance programs have been institutionalized to monitor ascendancies in the antimicrobial resistance curve and subsequently tackle it. Among these nationwide surveillance programs include Ocular Tracking Resistance in the US Today (Ocular TRUST) 34 , and Antibiotic Resistance Monitoring in Ocular Microorganisms (ARMOR) 35 , European Antimicrobial Resistance Surveillance System 36 , and Swedish Strategic Programme for the Rational Use of Antimicrobial Agents and Surveillance of Resistance 37 . However, in developing countries such as Ghana, aside from the limited accessibility to a national antimicrobial policy, there are compromise regulatory measures and poor adherence to the use of antibiotics 38 .
Multidrug resistance (MDR) is gradually gaining attention in mainstream medicine and public healthcare generally, as it renders antimicrobial agents ine cacious against pathogenic strains of bacteria. MDR causes delays in treatment and recoveries, rise in cost of therapy as well as increase in hospitalization time [39][40][41] . In a nationwide laboratory based surveillance studies in Ghana, Opintan et al reported over 70% prevalence of MDR against antibiotics commonly used in treating infections in Ghana 42 . This nding was consistent with studies conducted in the People's Republic of China 43,44 , Italy 45 , and Ethiopia 12 which showed similar increasing trends. Consequentially, without drastic measures, it is estimated that the world will experience over 10 million annual AMR-related deaths hence it has become imperative to devise ammunitions to curb the situation 46 . Importantly, a decline in ocular MDR will result in increased life expectancy as ocular resistance infections and associated blindness induce mortality.
There is a paucity of data on the prevalence and bacteria etiology of ocular infections in Ghana 9,27 . Furthermore, earlier microbiological investigations in Ghana did not exquisitely focus on ocular infections and associated microbes 42,47−49 . The absence of country-speci c contemporary estimates limits the modeling of future scenarios, and assumptions with unreliable data and/or making decisions with evidence from other countries is of questionable utility given the geographic differences. An insight on bacteria etiology of ocular infections presented by Ghanaian patients is critical for desirable choice of antibiotic therapy by clinicians. Therefore, the study aims to investigate the bacteria etiology of external ocular and periocular infections, and antimicrobial treatment patterns among a Ghanaian ophthalmic population. The isolates recovered from ocular specimen will aid future antibiotic sensitivity studies and also serve as a gateway for exploration of local medicinal plants as alternative therapeutic agents.

Results
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 signi cantly 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.
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 identi ed (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 identi ed 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 signi cantly associated with prevalence of bacterial infections (p > 0.05).
The novel study for the rst 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 cipro oxacin.
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 Ghana 2-4 . 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][14][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 America 26 . 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 signi cantly 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][14][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 ndings 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 signi cantly 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 ndings 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. Speci cally, 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 oralocular 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 nding 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 lthy 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. Speci cally, they induce cornea in ltration 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 cipro oxacin. 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, cipro oxacin a uoroquinolone 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 identi ed 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 studies 2,7,57 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 uorescent 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.

Conclusion
The prevalence of positive bacteria culture from external ocular and periocular infections was approximately 95%. Gram-negative organisms were commonly implicated and with Pseudomonas aeruginosa and Staphylococcus aureus as the predominant causative bacteria. Clinical presentations of conjunctivitis and keratitis infections were mostly caused by Pseudomonas aeruginosa and with polymyxin B, neomycin and cipro oxacin as the frequently administered antimicrobial therapy. Given the higher burden of ocular bacterial infections, measures (infections control program and antimicrobial agent management program) should be institutionalized to prevent emergence of resistant strains. We recommend future studies to focus on investigating into the potential antibiotic resistances infections within the Ghanaian ophthalmic population.

Study design, setting and population
A multi-center study was conducted among patients suspected of external ocular and periocular infections in three health facilities in Ghana, namely Anglican Eye Hospital, Jachie; St. Michaels Hospital, Pramso; and Kumasi South Hospital, Agogo from July 18, 2021 to September 18, 2021. Cornea scrapings and conjunctival specimens were obtained from infected eyes for bacteriological investigation together with collation of patients sociodemographic and clinical characteristics with a pretested structured questionnaire.

Study setting
The Anglican Eye Hospital (AEH), St. Michaels Hospital (SMH) and Kumasi South Hospital (KSH) were selected for the study primarily because of their higher out-patient-department (OPD) turnout and the anticipation of meeting our sample size target within the shortest time possible, as well as their wide catchment area and rural/urban interactions. The AEH and SMH are located in Bosomtwe; a rural district in Ghana whilst KSH is situated in the Asokwa municipal area, an urban settlement in the Ashanti Region of Ghana. All the facilities have either a permanent/visiting ophthalmologist, optometrists, ophthalmic nurses and opticians. All the facilities provide comprehensive eye services which range from case history, visual acuity assessment, refraction, dispensing of refractive glasses, management of anterior and posterior segment pathologies, prescribing of medications and performing scheduled surgeries. SMH and KSH, serve as immediate referral hospitals for the surrounding private and polyclinics. However, all clinical emergencies to the Komfo Anokye Teaching Hospital, the only tertiary health facility in the region. These facilities lack microbiology laboratory hence clinicians employ empirical approaches in their routine diagnosis and management of external ocular and periocular infections.

Study population and sampling
The study population involved patients who sought ophthalmic treatments/ services for external ocular and periocular infections at the eye clinics of the Anglican Eye Hospital, Jachie; St Michaels Hospital, Pramso; and the Kumasi South Hospital from July 18 to September 18, 2021. Patients presenting with signs and symptoms of external ocular and periocular infections were recruited for the study following a consent (and accent for minors). Patients reporting solely for optical correction, or participants on systemic/topical antibiotics or have performed ocular surgery in the last one week were excluded. A purposive sampling approach was used to recruit one hundred and fourteen (114) eligible subjects.

Study variables
The independent variables for this study were participants' sociodemographic factors; age, sex, ethnicity, religion, facility, socioeconomic; residence, highest level of education, occupation, marital status, health status; smoking habits, alcohol intake, systemic medical conditions and clinical characteristics (eyes affected, site of the eyes affected, risk factors, patient presenting symptoms) whereas the outcome/dependent variable was prevalence of bacteria ocular and periocular infections. Participants were assessed and clinical presentations classi ed based on operational terms reported previously 7 , and antimicrobial treatments documented accordingly.

Operational de nitions
Blepharitis in the study was characterized by gritty itchy sore eyes, with crusting and/or collarattes around the base of the eyelashes coupled with clogging of the Meibomian gland, loss of eyelashes and with demodex conjunctivitis. Conjunctivitis was de ned as conjunctival lesion delineated by hyperemia, chemosis, whitish tint purulent discharge and hemorrhage. Blepharoconjuntivitis presented as redness of the eye, with dry scaly eyelids and ensuing symptoms of itchiness and burning sensation. In keratoconjuntivitis, cornea and conjunctiva were implicated with complaints of dryness, itching and mucous discharge. Keratitis was de ned as lesion of the cornea with characteristic cornea edema, cellular in ltration, pain, redness, photophobia and ciliary injection. Hordeolum was de ned swelling and tenderness of the eyelid with acute pain, photophobia and mild epiphora. Ophthalmia neonatorum is a neonatal conjunctivitis presented within the rst 28 days of life with signs of eyelid edema, erythema and purulent discharge. Preseptal and orbital cellulitis showed similar features of painful swelling and/or tenderness of the eyelid with the later distinguished from the former by decreased vision and pain on eye motility.

Sociodemographic and clinical data
The patients sociodemographic, socioeconomic, and health status variables were gathered by the principal investigator and a trained research assistant using a pre-tested structured questionnaire. A comprehensive vision assessment including visual acuity, slit lamp biomicroscopy, and ophthalmoscopy was performed by a registered optometrist on all study participants. Subsequently, patient medical history, primary and secondary diagnosis, and antimicrobial therapy prescribed were extracted using a data collection form.

Specimen collection and transport
Overall, 103 ocular specimens were obtained from the eyes of patients with external ocular and periocular infections following aseptic procedures. With the patient eyes in an upward position of gaze conjunctival specimen were obtained by gently rolling a moistened saline cotton bud over the lower tarsal plate of the eyelids and fornix of the conjunctiva in repeated strokes, thus from nasal to temporal and vice versa. Samples from corneal ulcer and keratitis infections were obtained utilizing a modi ed version of an original protocol described previously 8 . Brie y, using slit-lamp biomicroscopy, and under topical local anesthesia (1-2 drops of 0.5% fresh proparacaine), edges of the ulcer were rmly scraped 8, 9,19 . On the contrary, none of the patients in our study presented with dacrocystitis and/or blepharitis hence a puncture and/or aspiration of the lacrimal sac as well as swabbing on the eyelids were not undertaken. The swabs were subsequently kept in a sterile freshly prepared nutrient broth and transported from the study site to the Microbiology Laboratory of the Faculty of Pharmacy and Pharmaceutical Sciences, Kwame Nkrumah University of Science and Technology for further microbial investigation.

Culture and identi cation of bacteria pathogens
All specimen obtained were initially inoculated on a Nutrient agar and incubated at 37°C for 24 hours and plates examined for growth afterwards. Plates with microbial growth were transferred onto various differential and selective media for preliminary isolation and identi cation. Speci cally, bacteria were cultured on a Mannitol Agar, MacConkey Agar, Bismuth sulphite (all from Oxoid Ltd. Basingstoke, Hants United Kingdom brand), Cetrimide agar (HiMedia Laboratories Pvt. Ltd Mumbai, India), 5% sheep Blood and Chocolate agars and incubated for 24 hours. Of note, with the exception of 5% blood and chocolate agars which were kept under anaerobic conditions, an aerobic atmosphere was maintained for all other differential agar media used. Conversely plates with no growth were re-incubated for additional 48 hours and consequently counted negative if no growth pattern appeared. In addition, microbial growth on differential media was again sub-cultured on a nutrient agar to obtained pure colonies and subsequently subjected to further phenotypic identi cation speci cally colony morphology, Gram stain, colony morphology and biochemical analyses. Gram-positive bacteria isolates were characterized using coagulase, catalase and bacitracin tests, whereas Gram-negative bacteria were differentiated using citrate utilization, lysine decarboxylase agar, indole and urease tests as well as triple sugar iron agar 31,58,59 . Details of the methodology are summarized in Figure 1.

Quality assurance and control
The questionnaires employed to gather the sociodemographic and clinical data were pretested at the Anglican Eye Hospital and revised accordingly following their feedback. Questionnaires were written in English and administered by the principal investigator and a trained research assistant. On the one hand, questionnaire was explained in local dialect for study subjects who could not comprehend instructions in English language. The data from study was doubled checked for accuracy and completeness. At the facility, all test tubes with ocular samples were well-labeled to avoid any mismatched. The laboratory reagents and culture media for the experiments were checked for expiry dates, and sterility control performed to ascertain the integrity of the media such as free from contamination. The media performance and/or functionality assessment was conducted using the American Type Culture Collection (ATCC) Standard Reference Strains. Speci cally, Escherichia. coli ATCC 25922; Pseudomonas aeruginosa ATCC 4853; Staphylococcus aureus ATCC 25923.

Data protection and management
The hardcopy version of the lled questionnaires was kept under lock and key and accessible only to the principal investigator and research advisor. Similarly, the softcopy of the non-aggregated dataset was protected using an alphanumeric stringed password. The research report presented to the respective facilities and for publication purposes were aggregated hence individual study participants could not be traced.

Ethical Consideration
To undertake this study a hierarchical ethical consideration protocols were followed. A written permission was sought from the authorities of the Anglican Eye Clinic, St. Michaels Hospital, and Kumasi South Hospital. The study protocol was then approved by the Committee on Human Research, Publication and Ethics (CHRPE), of the Kwame Nkrumah University of Science and Technology and the Komfo Anokye Teaching Hospital (Reference number: CHRPE/AP/282/21). Written informed consent was obtained from adult participants and for minors a written informed consent was taken from caregivers after study protocol was fully explained to the best of their comprehension. The study adhered to the tenets of the declaration of Helsinki 60 , and all laboratory procedures performed in accordance to the Clinical Laboratory Standard Institute guidelines, CLSI 61 .

Data was entered and managed in Microsoft Excel and further exported into Statistical Package and Service Solution version (IBM Corporation IBM® SPSS®
Statistics for Windows, version 25.0 Armonk, NY) compatible with windows. Normality assessment was performed using the Kolmogorov Smirnov statistic.
The demographics, socioeconomics, health status and clinical characteristics of the sample were presented and difference between males and females tested with chi-square analysis. Clinical diagnosis, cultural status and antimicrobial treatments were presented in cross tabulations using frequencies and percentages. Association between sample characteristics and prevalence of bacterial infections were investigated using bivariate logistic regression at a signi cance set at p<0.05.

Funding
The study received no speci c funding from public, private and/or non-pro t organization.

Availability of data materials
All relevant data and materials supporting the conclusion of this article is/are available within the manuscript and its supporting information les.

Ethical Consideration
To undertake this study a hierarchical ethical consideration protocols were followed. A written permission was sought from the authorities of the Anglican Eye Clinic, St. Michaels Hospital, and Kumasi South Hospital. The study protocol was then approved by the Committee on Human Research, Publication and Ethics (CHRPE), of the Kwame Nkrumah University of Science and Technology and the Komfo Anokye Teaching Hospital (Reference number: CHRPE/AP/282/21). Written informed consent was obtained from adult participants and for minors a written informed consent was taken from caregivers after study protocol was fully explained to the best of their comprehension. The study adhered to the tenets of the declaration of Helsinki 60 , and all laboratory procedures performed in accordance to the Clinical Laboratory Standard Institute guidelines, CLSI 61 .

Consent for publication
Not applicable

Competing interests
All authors declare no competing interests.             n, frequency; %, percentage frequency; CONS, Coagulase-negative staphylococcal species Table 5: Factors associated with external ocular and periocular infections among a Ghanaian ophthalmic population Flow diagram illustrating study methodology