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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 5  |  Issue : 1  |  Page : 39-42

Spectrum of bacterial conjunctivitis in Southern Pakistan: 10-year retrospective review of laboratory data


1 Department of Pathology and Laboratory Medicine, Aga Khan University, Karachi, Pakistan
2 Department of Surgery, Aga Khan University, Karachi, Pakistan
3 Department of Pathology and Laboratory Medicine; Department of Pediatrics and Child Health, Aga Khan University, Karachi, Pakistan

Date of Submission03-Sep-2020
Date of Acceptance26-Oct-2020
Date of Web Publication13-Mar-2021

Correspondence Address:
Dr. Tazeen Fatima
Department of Pathology and Laboratory Medicine, Aga Khan University, Stadium Road P. O. Box 3500, Karachi 74800
Pakistan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/bbrj.bbrj_165_20

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  Abstract 


Background: Bacterial conjunctivitis contributes largely to ocular morbidity in both developed and developing countries. The spectrum of conjunctivitis is influenced by geographic and climatic factors. One previous report from Pakistan had shown adenoviruses to be predominantly responsible for keratoconjunctivitis, however little is known about the bacterial agents responsible for conjunctivitis. In this study, we report the microbial etiology of bacterial conjunctivitis by performing a 10-year retrospective review of laboratory data. Methods: All conjunctival cultures received at the Aga Khan University Clinical Microbiology Laboratory from 2004 to 2013 with bacterial growth were identified through a laboratory database. Information on patients' demographic characteristics, identification of organisms, and antibiotic susceptibility was obtained from an archived database of laboratory records. Data were entered and analyzed in MS Excel. Results: A total of 1534 conjunctival culture samples were received at the clinical microbiology laboratory during the 10-year study period (2004–2013), of which 375 showed bacterial growth. Staphylococcus aureus was found to be the most common bacterial cause of conjunctivitis. Streptococcus pneumoniae was seen predominantly in children aged 0–14 years. Higher trends of resistance were noticed for trimethoprim-sulfamethoxazole and erythromycin. Conclusions: The bacterial profile of ocular surface cultures from patients with conjunctivitis showed prevalence of S. aureus in all ages and S. pneumoniae in children, with pseudomonal infections common in older age groups, likely associated with the use of contact lenses. Antibiotic susceptibility testing showed high level of resistance to topical antibiotics. Studies designed to address the challenges of antibiotic susceptibility testing against topical antibiotics are needed to inform empiric treatment guidelines in various age groups.

Keywords: Antimicrobial resistance, bacterial conjunctivitis, infants, Pakistan, Staphylococcus aureus, Streptococcus pneumoniae


How to cite this article:
Fatima T, Malik FR, Ahmed A, Khan E, Shakoor S. Spectrum of bacterial conjunctivitis in Southern Pakistan: 10-year retrospective review of laboratory data. Biomed Biotechnol Res J 2021;5:39-42

How to cite this URL:
Fatima T, Malik FR, Ahmed A, Khan E, Shakoor S. Spectrum of bacterial conjunctivitis in Southern Pakistan: 10-year retrospective review of laboratory data. Biomed Biotechnol Res J [serial online] 2021 [cited 2021 May 12];5:39-42. Available from: https://www.bmbtrj.org/text.asp?2021/5/1/39/311088




  Introduction Top


Visual impairment comprises a wide variety of infectious and noninfectious causes. Keratoconjunctivitis is the most common ocular disease, with a global incidence of 42.5%, and contributes largely to ocular morbidity in both developed and developing countries, being the fourth-leading cause of blindness worldwide.[1],[2],[3] There are various underlying causes of conjunctivitis, the prevalence of which depends on multiple factors including patient's age as well as the season of the year.[4] Viral etiology is by far the most common infectious cause of conjunctivitis, contributing to about 80% of all cases, with adenovirus being responsible for about 65% to 90% of the total cases.[4] The second-most common cause of infectious conjunctivitis is bacterial conjunctivitis, the incidence of which was estimated to be 132 in 10,000,[5] accounting for 50%–75% of all cases in children.[6] Cases of viral conjunctivitis are more commonly observed in summers, whereas that of bacterial conjunctivitis peak from December to April.[4] The spectrum of bacterial conjunctivitis is influenced by geographic, environmental, and climatic factors along with other predisposing factors such as ocular trauma, ocular surface disease, corneal surgery, and extensive use of contact lenses that also increase the likelihood of bacterial keratitis.[7] A previous report from Pakistan had shown adenoviruses to be predominantly responsible for keratoconjunctivitis,[8] however, little is known about bacterial pathogens responsible for conjunctivitis. Owing to the grave consequences of infectious conjunctivitis, prompt treatment with appropriate empirical antimicrobials is crucial. With the increasing incidence of infectious keratitis,[9] increasing antimicrobial resistance, and changing epidemiology, it is imperative to investigate the local spectrum of bacterial pathogens and antibiotic susceptibility patterns for evidence-based selection of empirical treatment regimens.

We set out to examine the microbial etiology of bacterial conjunctivitis and the antibiotic susceptibility and resistance patterns of recovered pathogens by carrying out a 10-year retrospective review of laboratory data from a central laboratory in Karachi, Pakistan.


  Methods Top


Ethics

This study was reviewed and granted a waiver of individual informed consent by the Ethical Review Committee of the Aga Khan University.

Study setting

This retrospective review was performed by examining records from the Aga Khan University Clinical Laboratories, a central laboratory situated in Karachi, Pakistan. The laboratory has over 271 collection units in various locations all over Pakistan, mostly concentrated however in the southern province of Sindh, and therefore receives samples for microbiological evaluation from representative locations across the south of Pakistan. The laboratory had ISO 9001:2000 certification during the study years.

Laboratory methods

Cultures and susceptibility testing at the Aga Khan University clinical microbiology laboratory were performed according to the standards set by the American Society for Microbiology[10] and the Clinical and Laboratory Standards Institute (CLSI) documents,[11] respectively. Antibiotics commonly used as topical ophthalmic solutions and ointments, that is, chloramphenicol (CHL), ofloxacin (OFX), gentamicin (GEN), polymyxin B (PB), trimethoprim-sulfamethoxazole (TSX), and erythromycin (ERY), were included in the analysis. As CLSI does not recommend breakpoints for topical application, breakpoints for systemic infections were used for determining susceptibility.

Data retrieval and analysis

Laboratory record archives from all conjunctival swabs received and performed at the Aga Khan University Clinical Microbiology Laboratory from January 2004 to December 2013 were retrospectively reviewed. Laboratory parameters available in the records included patient's name, age, and sex; date of specimen collection; date of receipt in laboratory; date of reporting; bacteria or fungi cultured; and antibiotic susceptibilities. No clinical history was recorded in the archives, however laboratory physicians routinely accessed clinical records from the requesting physicians, and added relevant comments in the reports, identifying the etiologic significance of the cultured isolates.

A database was created in MS Excel, and quality checked for completeness of information, removal of duplicates, and system errors. Patient identification was removed from the analysis database to maintain confidentiality. Frequencies and percentages were calculated in MS Excel.

Analysis of bacterial isolation by age was performed according to the following age quintiles: <1 year, 1–2 years, 3–14 years, 15–38 years, and >39 years. To determine significant difference between pathogen proportions across age groups, Chi-square 5-sample test was carried out for equality of proportions using an online calculator at www.socscistatistics.com.


  Results Top


A total of 1534 conjunctival swab samples were received at the clinical microbiology laboratory site in the 10-year period (2004–2013). Of these, 375 (24.4%) samples showed bacterial growth, while the remaining 1159 (75.6%) were negative for any bacteria or fungi. Culture of the 375 specimens yielded 395 organisms, with 4.3% (n = 16) of the specimens yielding polymicrobial results. The susceptibility results were analyzed for all the 395 isolates in the 375 cultured specimens.

Among the 375 culture-positive specimens, 174 (46.4%) were from females, whereas 201 (53.6%) were from males. Analysis of age distribution of the samples showed that 19.6% of all the samples (n = 302) and 38.9% of positive samples (n = 146) were from infants, with a positivity rate of 48.3% among infants.

Of the 395 organisms cultured, 182 were Gram-positive, 211 were Gram-negative, and 2 were fungi. Proportion of the isolated organisms by year of isolation is shown in [Figure 1]. No significant differences or consistent trends were observed in the rates of isolation of organisms.
Figure 1: Proportion of isolation of organisms among positive conjunctival swab cultures. Staphylococcus aureus remained consistently common, followed by Streptococcus pneumoniae and Pseudomonas aeruginosa. SA: Staphylococcus aureus, SPN: Streptococcus pneumoniae, PA: Pseudomonas aeruginosa, EGNB: Enteric Gram-negative bacilli, PSP: Pseudomonas species, HI/P: Haemophilus influenzae and parainfluenzae, ACSP: Acinetobacter species, MC: Moraxella catarrhalis, STRSP: Streptococcus species (including beta-hemolytic Streptococci), MISC: Miscellaneous (organisms included Aeromonas species, Bacillus species, Corynebacterium species, Burkholderia cepacia, Stenotrophomonas maltophilia, Neisseria gonorrheae, Candida parapsilosis, and Fusarium species)

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The most frequently isolated organism was Staphylococcus aureus which accounted for 24.8% (n = 98) of the total bacterial isolates. The second common organism was Streptococcus pneumoniae with 17.2% (n = 68) of the total, followed by Pseudomonas aeruginosa with 16.2% (n = 64) isolation. When analyzed by age quintiles, as shown in [Table 1], no specific trends were observed and the same organisms remained prevalent across all age groups, except S. pneumoniae which was observed in greater proportions in children.
Table 1: Relative proportions of pathogens among positive eye swab cultures, 2004-2013, with 5-sample test of equivalence of proportions

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Antibiotic susceptibility to common topical agents

Highest resistance rates were seen for TSX (36%) throughout the study period consistently, followed by ERY (10.1%) which increased gradually over time. Pathogen resistance against GEN, OFX, and CHL was observed in 9.1%, 6.9%, and 5.8% of isolates, respectively. PB was tested in only one-fourth of the pathogens, which showed a low resistance of only 0.8%.


  Conclusions Top


Prompt diagnosis and early commencement of appropriate treatment is essential to accomplish quick resolution of bacterial conjunctivitis to minimize the risk of corneal infection. Microbiological cultures of conjunctival samples remain the cornerstone for diagnosis, along with antibiotic sensitivity testing for proper selection of effective antibiotics against the causative microorganism. However, culture facilities are not always available or affordable in resource-limited settings. Furthermore, the microbial spectrum varies with age groups and other risk factors. Information on regional microbial trends and antimicrobial resistance can be used to guide for the best empirical antibiotic choices. We investigated the bacterial spectrum and antibiotic susceptibility patterns in patients with bacterial conjunctivitis over a 10-year period (2004–2013) in southern Pakistan.

S. aureus was found to be the most frequently isolated bacterial pathogen across all ages and in all years. This finding is similar to a recent study from India which shares its border with Pakistan[5] but differs from Iran where a systematic review reported high rates of S. aureus infections but reported coagulase-negative Staphylococci (CONS) to be the most prevalent pathogen.[12] We did not find any CONS infections in our retrospective review, but this may have been due to conflicting guidance regarding the pathogen status of CONS. Recent data have shown that CONS are the most prevalent normal flora in the human eye[13],[14] (N13, N14); although there are instances of isolation of some pathogenic bacteria from healthy human eyes, the prevalence of CONS far outweighs that of these pathogens.

Different studies from Asia, San Francisco, South Korea, and South India reported P. aeruginosa as the most common Gram-negative rod to be responsible for bacterial keratoconjunctivitis, which is also in accordance with our findings.[3],[7],[9],[15] The highest pseudomonas infections in our data were observed in female young adults. This may be linked with higher rates of contact lens use among adults.

S. pneumoniae infection has been associated with poor visual outcomes in various studies.[16] A large multicenter study from Asia in 2018 reported S. pneumoniae to be the most common Gram-positive bacteria implicated in bacterial keratitis with an incidence of 6.3%.[16] Another study from India reported an incidence of 11.6%.[15] A fairly higher frequency was recorded in our cohort of 19%. One plausible reason for the higher incidence of S. pneumoniae infections in the Asian population could be nonadherence to immunization. Although the protection against conjunctivitis conferred by the pneumococcal conjugate vaccine (PCV) is questionable, there is some data to suggest that PCV decreases the incidence of pneumococcal conjunctivitis caused by vaccine serotypes.[17] Overcrowding, poor hygiene, and living conditions also contribute to higher incidence of pneumococcal infections.[18] Pneumococcal infections were predominantly seen in children, with decreasing incidence thereafter. Haemophilus influenzae/parainfluenzae infections were also frequent in children below 2 years of age.

Essa Abdullah et al. reported a resistance rate of 29.3% for TSX among Gram-positive isolates in conjunctival samples.[19] We report a resistance rate of 36%, which may be an indication of increasing drug resistance. Yet, the resistance rates for ERY (10.1%), GEN (9.1%), and CHL (5.8%) are lower as compared to that of other studies where rates ranging from 7% to 45% for CHL, 13% to 22% for GEN, and around 58% to 72% for ERY[9],[16],[18],[19],[20] have been reported.

Our study has several notable limitations. We performed a retrospective review of laboratory data and therefore proportions of bacterial pathogens recovered cannot inform the relative incidence. As mentioned earlier, interpretation of susceptibility testing results was performed as per the CLSI standards which do not have specific breakpoints for conjunctival infections or for topical use of antibiotics. Our review ended in 2013, and therefore may not be representative of the pathogen proportions or resistance rates from recent years.

Routine use of laboratory data from quality-assured laboratories can provide a proxy for prospective observational studies on conjunctivitis. Nevertheless, due to the limitations noted above, well-designed studies should be performed to obtain empirical evidence to inform the use of topical antibiotics in bacterial conjunctivitis. With variations in bacterial spectrum and antibiotic susceptibility, it is important to emphasize the importance of culture and antibiotic sensitivity testing in all infectious ocular diseases.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Lin A, Rhee MK, Akpek EK, Amescua G, Farid M, Garcia-Ferrer FJ, et al. Bacterial Keratitis Preferred Practice Pattern®. Ophthalmology 2019;126:P1-55.  Back to cited text no. 1
    
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Fatima K, Shahid E, Shaikh A. Frequency of common eye diseases in pediatric outpatient department of a tertiary care hospital. Pak J Ophthalmol 2015;31:154-7.  Back to cited text no. 2
    
3.
Khor WB, Prajna VN, Garg P, Mehta JS, Xie L, Liu Z, et al. The Asia Cornea Society Infectious Keratitis Study: A prospective multicenter study of infectious keratitis in Asia. Am J Ophthalmol 2018;195:161-70.  Back to cited text no. 3
    
4.
Azari AA, Barney NP. Conjunctivitis: A systematic review of diagnosis and treatment. JAMA 2013;310:1721-9.  Back to cited text no. 4
    
5.
Math SS, Rauth SG. Study of organisms isolation from acute bacterial conjunctivitis cases. Indian Journal of Clinical and Experimental Ophthalmology 2019;5:318-21.  Back to cited text no. 5
    
6.
Høvding G. Acute bacterial conjunctivitis. Acta Ophthalmol 2008;86:5-17.  Back to cited text no. 6
    
7.
Peng MY, Cevallos V, McLeod SD, Lietman TM, Rose-Nussbaumer J. Bacterial Keratitis: Isolated Organisms and Antibiotic Resistance Patterns in San Francisco. Cornea 2018;37:84-7.  Back to cited text no. 7
    
8.
Woodland RM, Darougar S, Thaker U, Cornell L, Siddique M, Wania J, et al. Causes of conjunctivitis and keratoconjunctivitis in Karachi, Pakistan. Trans R Soc Trop Med Hyg 1992;86:317-20.  Back to cited text no. 8
    
9.
Mun Y, Kim MK, Oh JY. Ten-year analysis of microbiological profile and antibiotic sensitivity for bacterial keratitis in Korea. PLoS One 2019;14:e0213103.  Back to cited text no. 9
    
10.
Isenberg HD. Clinical Microbiology Procedures Handbook. USA: ASM Press; 2004.  Back to cited text no. 10
    
11.
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Informational Supplements. Clinical and Laboratory Standards Institute; 2004-2013. p. M100.  Back to cited text no. 11
    
12.
Teweldemedhin M, Gebreyesus H, Atsbaha AH, Asgedom SW, Saravanan M. Bacterial profile of ocular infections: A systematic review. BMC Ophthalmol 2017;17:212.  Back to cited text no. 12
    
13.
Capriotti JA, Pelletier JS, Shah M, Caivano DM, Ritterband DC. Normal ocular flora in healthy eyes from a rural population in Sierra Leone. Int Ophthalmol 2009;29:81-4.  Back to cited text no. 13
    
14.
Sthapit PR, Tuladhar NR. Conjunctival flora of normal human eye. JSM Ophthalmol 2014;2:1021.  Back to cited text no. 14
    
15.
Lalitha P, Manoharan G, Karpagam R, Prajna NV, Srinivasan M, Mascarenhas J, et al. Trends in antibiotic resistance in bacterial keratitis isolates from South India. Br J Ophthalmol 2017;101:108-13.  Back to cited text no. 15
    
16.
Green MD, Apel AJ, Naduvilath T, Stapleton FJ. Clinical outcomes of keratitis. Clin Exp Ophthalmol 2007;35:421-6.  Back to cited text no. 16
    
17.
Howard LM, de St Maurice A. Unraveling the Impact of Pneumococcal Conjugate Vaccines on Bacterial Conjunctivitis in Children. Clin Infect Dis 2020.  Back to cited text no. 17
    
18.
Benton AH, Marquart ME. The role of pneumococcal virulence factors in ocular infectious diseases. Interdisciplinary Perspectives on Infectious Diseases 2018.  Back to cited text no. 18
    
19.
Essa Abdullah F, Irfan Khan M, Waheed S. Current pattern of antibiotic resistance of clinical isolates among conjunctival swabs. Pak J Med Sci 2013;29:81-4.  Back to cited text no. 19
    
20.
Deguchi H, Kitazawa K, Kayukawa K, Kondoh E, Fukumoto A, Yamasaki T, et al. The trend of resistance to antibiotics for ocular infection of Staphylococcus aureus, coagulase-negative Staphylococci, and Corynebacterium compared with 10-years previous: A retrospective observational study. PLoS One 2018;13:e0203705.  Back to cited text no. 20
    


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