Emergence and Spread of Multidrug Resistance in Ocular Bacterial Pathogens: A Current Update

  • Sarim Ahmad
  • Shamim Ahmad
  • Faizan Abul Qais
  • Mohammad Shavez Khan
  • Iqbal Ahmad


The tremendous increase of multidrug-resistant bacterial pathogens has posed a serious threat in the management of infectious diseases. The human eye is known to commensally host the normal flora, including the opportunistic pathogens. The researchers have isolated and characterized numerous microbes belonging to different genera from healthy eye, including Pseudomonas, Propionibacterium, Acinetobacter, Corynebacterium, Brevundimonas, Staphylococcus, Sphyngomonas, Streptococcus, and many others. The human eye is virtually impermeable to microbes, despite being exposed to an array of microorganisms. Ocular infections usually occur through invasion of microbes that may come either from bloodstream or by breaching the ocular barriers. Both gram-negative and gram-positive bacteria are known to be responsible for ocular infections, with the major causative gram-positive bacteria being S. pneumoniae, coagulase-negative staphylococci, S. aureus, and S. pyogenes, with N. gonorrhoeae, Moraxella spp., P. aeruginosa, K. pneumoniae, E. coli, and Proteus spp. also being commonly isolated. Apart from the unchecked use of antibiotics and the dissemination of multidrug-resistant bacteria, development of biofilms on ocular surfaces are also a major concern for antimicrobial resistance. In biofilms, the antibiotics are less likely to penetrate, due to reduced rates of diffusions making some of the cells in biofilms more resistant, and eventually increasing the effective antibiotic dose by many folds in comparison to planktonic mode cells. In this chapter, a survey on the emergence and spread of MDR ocular bacterial pathogens has been made.


Ocular pathogens Ocular infections Multidrug resistance MDR Biofilm 


  1. Adán, A., Casaroli-Marano, R. P., Gris, O., et al. (2008). Pathological findings in the lens capsules and intraocular lens in chronic pseudophakic endophthalmitis: An electron microscopy study. Eye, 22, 113–119. Scholar
  2. Ahmad, I., Khan, M. S., Altaf, M. M., et al. (2017). Biofilms: An overview of their significance in plant and soil health. In Biofilms in plant and soil health (pp. 1–25). Chichester: John Wiley & Sons, Ltd.CrossRefGoogle Scholar
  3. Al-Dhaheri, H. S., Al-Tamimi, M. D., Khandekar, R. B., et al. (2016). Ocular pathogens and antibiotic sensitivity in bacterial keratitis isolates at king Khaled eye specialist hospital, 2011 to 2014. Cornea, 35, 789–794. Scholar
  4. Alexandrakis, G. (2000). Shifting trends in bacterial keratitis in South Florida and emerging resistance to fluoroquinolones. Ophthalmology, 107, 1497–1502. Scholar
  5. Amsalu, A., Abebe, T., Mihret, A., et al. (2015). Potential bacterial pathogens of external ocular infections and their antibiotic susceptibility pattern at Hawassa university teaching and referral hospital, southern Ethiopia. African Journal of Microbiology Research, 9, 1012–1019. Scholar
  6. Asbell, P. A., & Sanfilippo, C. M. (2017). Antibiotic resistance trends among ocular pathogens in the US—Cumulative results from the antibiotic resistance monitoring in ocular microorganisms (ARMOR) surveillance study. US Ophthalmic Review, 10, 35–38. Scholar
  7. Asbell, P. A., Colby, K. A., Deng, S., et al. (2008a). Ocular TRUST: Nationwide antimicrobial susceptibility patterns in ocular isolates. American Journal of Ophthalmology, 145, 951–958.e1. Scholar
  8. Asbell, P. A., Sahm, D. F., Shaw, M., et al. (2008b). Increasing prevalence of methicillin resistance in serious ocular infections caused by Staphylococcus aureus in the United States: 2000 to 2005. Journal of Cataract and Refractive Surgery, 34, 814–818. Scholar
  9. Asbell, P. A., Pandit, R. T., & Sanfilippo, C. M. (2018). Antibiotic resistance rates by geographic region among ocular pathogens collected during the ARMOR surveillance study. Ophthalmology and therapy, 7, 417. Scholar
  10. Ashley, D. J. B., & Brindle, M. J. (1960). Penicillin resistance in staphylococci isolated in a casualty department. Journal of Clinical Pathology, 13, 336–338. Scholar
  11. Azari, A. A., & Barney, N. P. (2013). Conjunctivitis: A systematic review of diagnosis and treatment. JAMA, 310, 1721–1730. Scholar
  12. Baillif, S., Casoli, E., Marion, K., et al. (2006). A novel in vitro model to study staphylococcal biofilm formation on intraocular lenses under hydrodynamic conditions. Investig Opthalmology Vis Sci, 47, 3410–3416. Scholar
  13. Baillif, S., Ecochard, R., Casoli, E., et al. (2008). Adherence and kinetics of biofilm formation of Staphylococcus epidermidis to different types of intraocular lenses under dynamic flow conditions. Journal of Cataract and Refractive Surgery, 34, 153–158. Scholar
  14. Bausz, M., Fodor, E., Resch, M. D., & Kristóf, K. (2006). Bacterial contamination in the anterior chamber after povidone–iodine application and the effect of the lens implantation device. Journal of Cataract and Refractive Surgery, 32, 1691–1695. Scholar
  15. Bertino, J. S. (2009). Impact of antibiotic resistance in the management of ocular infections: The role of current and future antibiotics. Clinical Ophthalmology, 3, 507–521.CrossRefGoogle Scholar
  16. Bharathi, M. J., Amuthan, M., Viswanathan, S., et al. (2010a). Prevalence of bacterial pathogens causing ocular infections in South India. Indian Journal of Pathology & Microbiology, 53, 281–286. Scholar
  17. Bharathi, M. J., Ramakrishnan, R., Shivakumar, C., et al. (2010b). Etiology and antibacterial susceptibility pattern of community-acquired bacterial ocular infections in a tertiary eye care hospital in South India. Indian Journal of Ophthalmology, 58, 497–507. Scholar
  18. Bispo, P., Haas, W., & Gilmore, M. (2015). Biofilms in infections of the eye. Pathogens, 4, 111–136. Scholar
  19. Blair, J. M. A., Webber, M. A., Baylay, A. J., et al. (2015). Molecular mechanisms of antibiotic resistance. Nature Reviews. Microbiology, 13, 42–51. Scholar
  20. Brown, L. (2007). Resistance to ocular antibiotics: An overview. Clinical & Experimental Optometry, 90, 258–262. Scholar
  21. Chalita, M. R., Höfling-Lima, A. L., Paranhos, A., et al. (2004). Shifting trends in in vitro antibiotic susceptibilities for common ocular isolates during a period of 15 years. American Journal of Ophthalmology, 137, 43–51. Scholar
  22. Chambers, H. F. (1997). Methicillin resistance in staphylococci: Molecular and biochemical basis and clinical implications. Clinical Microbiology Reviews, 10, 781–791. Scholar
  23. Chang, V. S., Dhaliwal, D. K., Raju, L., & Kowalski, R. P. (2015). Antibiotic resistance in the treatment of Staphylococcus aureus keratitis: A 20-year review. Cornea, 34, 698–703. Scholar
  24. Chaudhary, M., Bhattarai, A., Adhikari, S., & Bhatta, D. (2010). Bacteriology and antimicrobial susceptibility of adult chronic dacryocystitis. Nepalese Journal of Ophthalmology, 2, 105–113. Scholar
  25. Chaudhry, N. A., Flynn, H. W., Murray, T. G., et al. (1999). Emerging ciprofloxacin-resistant Pseudomonas aeruginosa. American Journal of Ophthalmology, 128, 509–510. Scholar
  26. Cheng, D. (2007). Relationship of quantitative structure and pharmacokinetics in fluoroquinolone antibacterials. World Journal of Gastroenterology, 13, 2496–2503. Scholar
  27. Chew, F. L., Soong, T., Shin, H. C., et al. (2010). Topical piperacillin/Tazobactam for recalcitrant Pseudomonas Aeruginosa keratitis. Journal of Ocular Pharmacology and Therapeutics, 26, 219–222. Scholar
  28. Davies, D. (2003). Understanding biofilm resistance to antibacterial agents. Nature Reviews. Drug Discovery, 2, 114–122. Scholar
  29. de Caro, J. J., Ta, C. N., Ho, H.-K. V., et al. (2008). Bacterial contamination of ocular surface and needles in patients undergoing intravitreal injections. Retina, 28, 877–883. Scholar
  30. Deguchi, H., Kitazawa, K., Kayukawa, K., et al. (2018). 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, 13, e0203705. Scholar
  31. Dong, Q., Brulc, J. M., Iovieno, A., et al. (2011). Diversity of Bacteria at healthy human conjunctiva. Investigative Opthalmology & Visual Science, 52, 5408–5413. Scholar
  32. Dongari-Bagtzoglou, A. (2008). Pathogenesis of mucosal biofilm infections: Challenges and progress. Expert Review of Anti-Infective Therapy, 6, 201–208. Scholar
  33. Donlan, R. M. (2001). Biofilm formation: A clinically relevant microbiological process. Clinical Infectious Diseases, 33, 1387–1392. Scholar
  34. Donlan, R. M. (2002). Biofilms: Microbial life on surfaces. Emerging Infectious Diseases, 8, 881–890. Scholar
  35. Douglas, L. J. (2002). Medical importance of biofilms in Candida infections. Revista Iberoamericana de Micología, 19, 139–143.PubMedGoogle Scholar
  36. Doyle, A., Beigi, B., Early, A., et al. (1995). Adherence of bacteria to intraocular lenses: A prospective study. The British Journal of Ophthalmology, 79, 347–349. Scholar
  37. Durand, M. L. (2013). Endophthalmitis. Clinical Microbiology and Infection, 19, 227–234. Scholar
  38. Eguchi, H., Kuwahara, T., Miyamoto, T., et al. (2008). High-level fluoroquinolone resistance in ophthalmic clinical isolates belonging to the species Corynebacterium macginleyi. Journal of Clinical Microbiology, 46, 527–532. Scholar
  39. Enright, M. C., Robinson, D. A., Randle, G., et al. (2002). The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proceedings of the National Academy of Sciences, 99, 7687–7692. Scholar
  40. Fey, P. D., & Olson, M. E. (2010). Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiology, 5, 917–933. Scholar
  41. Fintelmann, R. E. (2011). Topical fluoroquinolone use as a risk factor for in vitro fluoroquinolone resistance in ocular cultures. Archives of Ophthalmology, 129, 399–402. Scholar
  42. Fukuda, M., Ohashi, H., Matsumoto, C., et al. (2002). Methicillin-resistant Staphylococcus aureus and methicillin-resistant coagulase-negative Staphylococcus ocular surface infection. Cornea, 21, S86–S89. Scholar
  43. Funke, G., Pagano-Niederer, M., & Bernauer, W. (1998). Corynebacterium macginleyi has to date been isolated exclusively from conjunctival swabs. Journal of Clinical Microbiology, 36, 3670–3673.PubMedPubMedCentralGoogle Scholar
  44. Ganguly, N. K., Arora, N. K., Chandy, S. J., et al. (2011). Rationalizing antibiotic use to limit antibiotic resistance in India. The Indian Journal of Medical Research, 134, 281–294.PubMedGoogle Scholar
  45. Garcı́a-Sáenz, M. C., Arias-Puente, A., Fresnadillo-Martinez, M. J., & Matilla-Rodriguez, A. (2000). In vitro adhesion of Staphylococcus epidermidis to intraocular lenses. Journal of Cataract and Refractive Surgery, 26, 1673–1679. Scholar
  46. Getahun, E., Gelaw, B., Assefa, A., et al. (2017). Bacterial pathogens associated with external ocular infections alongside eminent proportion of multidrug resistant isolates at the University of Gondar Hospital, Northwest Ethiopia. BMC Ophthalmology, 17, 151. Scholar
  47. Goldstein, M. H., Kowalski, R. P., & Gordon, Y. J. (1999). Emerging fluoroquinolone resistance in bacterial keratitis. Ophthalmology, 106, 1213–1318. Scholar
  48. Graham, J. E., Moore, J. E. J. E., Jiru, X., et al. (2007). Ocular pathogen or commensal: A PCR-based study of surface bacterial Flora in Normal and dry eyes. Investigative Ophthalmology and Visual Science, 48, 5616. Scholar
  49. Haas, J., Larson, E., Ross, B., et al. (2005). Epidemiology and diagnosis of hospital-acquired conjunctivitis among neonatal intensive care unit patients. The Pediatric Infectious Disease Journal, 24, 586–589.CrossRefGoogle Scholar
  50. Haas, W., Pillar, C. M., Zurenko, G. E., et al. (2009). Besifloxacin, a novel fluoroquinolone, has broad-Spectrum in vitro activity against aerobic and anaerobic Bacteria. Antimicrobial Agents and Chemotherapy, 53, 3552–3560. Scholar
  51. Haas, W., Pillar, C. M., Torres, M., et al. (2011). Monitoring antibiotic resistance in ocular microorganisms: Results from the antibiotic resistance monitoring in ocular MicRorganisms (ARMOR) 2009 surveillance study. American Journal of Ophthalmology, 152, 567–574.e3. Scholar
  52. Hall-Stoodley, L., Costerton, J. W., & Stoodley, P. (2004). Bacterial biofilms: From the natural environment to infectious diseases. Nature Reviews. Microbiology, 2, 95–108. Scholar
  53. Harper, T., Miller, D., & Flynn, H. W. (2007). In vitro efficacy and Pharmacodynamic indices for antibiotics against coagulase-negative Staphylococcus Endophthalmitis isolates. Ophthalmology, 114, 871–875. Scholar
  54. Hemavathi, Pooja, S., & Poornima, S. (2014). Profile of microbial isolates in ophthalmic infections and antibiotic susceptibility of the bacterial isolates: A study in an eye care hospital, Bangalore. Journal of Clinical and Diagnostic Research, 8, 23–25. Scholar
  55. Hirota, K., Murakami, K., Nemoto, K., & Miyake, Y. (2005). Coating of a surface with 2-methacryloyloxyethyl phosphorylcholine (MPC) co-polymer significantly reduces retention of human pathogenic microorganisms. FEMS Microbiology Letters, 248, 37–45. Scholar
  56. Ho, V., Ho, L. Y., Ranchod, T. M., et al. (2011). Endogenous methicillin-resistant Staphylococcus aureus endophthalmitis. Retina, 31, 596–601. Scholar
  57. Høvding, G. (2009). The conjunctival and contact lens bacterial flora during lens wear. Acta Ophthalmologica, 59, 387–401. Scholar
  58. Huang, X.-D., Yao, K., Zhang, H., et al. (2007). Surface modification of silicone intraocular lens by 2-methacryloyloxyethyl phosphoryl-choline binding to reduce Staphylococcus epidermidis adherence. Clinical & Experimental Ophthalmology, 35, 462–467. Scholar
  59. Hwang, D. G. (2004). Fluoroquinolone resistance in ophthalmology and the potential role for newer ophthalmic fluoroquinolones. Survey of Ophthalmology, 49, S79–S83. Scholar
  60. Iwalokun, B. A., Oluwadun, A., Akinsinde, K. A., et al. (2011). Bacteriologic and plasmid analysis of etiologic agents of conjunctivitis in Lagos, Nigeria. Journal of Ophthalmic Inflammation and Infection, 1, 95–103. Scholar
  61. Jevons, M., Coe, A., & Parker, M. (1963). Methicillin resistance in staphylococci. Lancet, 281, 904–907.CrossRefGoogle Scholar
  62. Joussen, A. M. (2000). Corynebacterium macginleyi: A conjunctiva specific pathogen. The British Journal of Ophthalmology, 84, 1420–1422. Scholar
  63. Juarez-Verdayes, M. A., Ramon-Perez, M. L., Flores-Paez, L. A., et al. (2013). Staphylococcus epidermidis with the icaA−/icaD-/IS256- genotype and protein or protein/extracellular-DNA biofilm IS frequent in ocular infections. Journal of Medical Microbiology, 62, 1579–1587. Scholar
  64. Kaistha, S., Singh, S., & Katiyar, R. (2011). High oxacillin, vancomycin and fluoroquinolone resistance amongst biofilm forming Staphylococcus aureus isolates from ulcerative keratitis infections. Indian Journal of Medical Microbiology, 29, 312–313. Scholar
  65. Kaliamurthy, J., Nelson Jesudasan, C. A., Geraldine, P., et al. (2005). Comparison of in vitro susceptibilities of ocular bacterial isolates to Gatifloxacin and other topical antibiotics. Ophthalmic Research, 37, 117–122. Scholar
  66. Kennedy, K., & Collignon, P. (2010). Colonisation with Escherichia coli resistant to “critically important” antibiotics: A high risk for international travellers. European Journal of Clinical Microbiology & Infectious Diseases, 29, 1501–1506. Scholar
  67. Khan, M. S. A., Ahmad, I., Sajid, M., & Cameotra, S. S. (2014). Current and emergent control strategies for medical biofilms. In K. P. Rumbaugh & I. Ahmad (Eds.), Antibiofilm agents (pp. 117–159). Heidelberg: Springer Nature.CrossRefGoogle Scholar
  68. Khosravi, A., Mehdinejad, M., & Heidari, M. (2007). Bacteriological findings in patients with ocular infection and antibiotic susceptibility patterns of isolated pathogens. Singapore Medical Journal, 48, 741–743.PubMedGoogle Scholar
  69. Larkin, D. F. P., & Leeming, J. P. (1991). Quantitative alterations of the commensal eye bacteria in contact lens wear. Eye, 5, 70–74. Scholar
  70. Lee, S. H., Oh, D. H., Jung, J. Y., et al. (2012). Comparative ocular microbial communities in humans with and without blepharitis. Investigative Ophthalmology and Visual Science, 53, 5585–5593. Scholar
  71. Leitch, E. C., Harmis, N. Y., Corrigan, K. M., & Willcox, M. D. (1998). Identification and enumeration of staphylococci from the eye during soft contact lens wear. Optometry and Vision Science, 75, 258–265.CrossRefGoogle Scholar
  72. Locatelli, C. I., Kwitko, S., & Simonetti, A. B. (2003). Conjunctival endogenous microbiota in patients submitted to cataract surgery. Brazilian Journal of Microbiology, 34, 203–209. Scholar
  73. Major, J. C., Engelbert, M., Flynn, H. W., et al. (2010). Staphylococcus aureus Endophthalmitis: Antibiotic susceptibilities, methicillin resistance, and clinical outcomes. American Journal of Ophthalmology, 149, 278–283.e1. Scholar
  74. Makki, A. R., Sharma, S., Duggirala, A., et al. (2011). Phenotypic and genotypic characterization of coagulase negative staphylococci (CoNS) other than Staphylococcus epidermidis isolated from ocular infections. Investigative Ophthalmology and Visual Science, 52, 9018. Scholar
  75. Maneesh, P.-S., Sowmiya, M., Bharani, T., et al. (2016). Characterization of antibiotic resistance profiles of ocular Enterobacteriaceae isolates. European journal of microbiology & immunology, 6, 40–48. Scholar
  76. Marangon, F. B., Miller, D., Muallem, M. S., et al. (2004). Ciprofloxacin and levofloxacin resistance among methicillin-sensitive staphylococcus aureus isolates from keratitis and conjunctivitis. American Journal of Ophthalmology, 137, 453–458. Scholar
  77. Mayo, M. S., Cook, W. L., Schlitzer, R. L., et al. (1986). Antibiograms, serotypes, and plasmid profiles of Pseudomonas aeruginosa associated with corneal ulcers and contact lens wear. Journal of Clinical Microbiology, 24, 372–376.PubMedPubMedCentralGoogle Scholar
  78. McDonald, M., & Blondeau, J. M. (2010). Emerging antibiotic resistance in ocular infections and the role of fluoroquinolones. Journal of Cataract and Refractive Surgery, 36, 1588–1598. Scholar
  79. Melo, G. B., Bispo, P. J. M., Yu, M. C. Z., et al. (2011). Microbial profile and antibiotic susceptibility of culture-positive bacterial endophthalmitis. Eye, 25, 382–388. Scholar
  80. Miller, D. (2006). In vitro fluoroquinolone resistance in staphylococcal Endophthalmitis isolates. Archives of Ophthalmology, 124, 479–483. Scholar
  81. Miller, D. (2017). Update on the epidemiology and antibiotic resistance of ocular infections. Middle East African journal of ophthalmology, 24, 30–42. Scholar
  82. Miño de Kaspar, H., Kreutzer, T. C., Aguirre-Romo, I., et al. (2008). A Prospective Randomized Study to Determine the Efficacy of Preoperative Topical Levofloxacin in Reducing Conjunctival Bacterial Flora. American Journal of Ophthalmology, 145, 136–142.e2. Scholar
  83. Mistlberger, A., Ruckhofer, J., Raithel, E., et al. (1997). Anterior chamber contamination during cataract surgery with intraocular lens implantation. Journal of Cataract and Refractive Surgery, 23, 1064–1069. Scholar
  84. Morrissey, I., Burnett, R., VILJOEN, L., & ROBBINS, M. (2004). Surveillance of the susceptibility of ocular bacterial pathogens to the fluoroquinolone gatifloxacin and other antimicrobials in Europe during 2001/2002. The Journal of Infection, 49, 109–114. Scholar
  85. Mulla, S. A., Khokhar, N. D., & Revdiwala, S. B. (2012). Ocular infections: Rational approach to antibiotic therapy. National Journal of Medical Research, 2, 22–24.Google Scholar
  86. Muluye, D., Wondimeneh, Y., Moges, F., et al. (2014). Types and drug susceptibility patterns of bacterial isolates from eye discharge samples at Gondar University hospital, Northwest Ethiopia. BMC Research Notes, 7, 292. Scholar
  87. Namitha, B. N. B., Mahalakshmi, Auchat, R., et al. (2014). Aerobic bacteriological profile in cases of ocular infections in a tertiary care hospital (Navodaya Medical College & Research Centre, Raichur). IOSR Journal of Dental and Medical Sciences, 13, 14–21.Google Scholar
  88. Nazeerullah, R., Sarite, S., & Musa, A. (2014). Bacterial profile and antimicrobial susceptibility pattern of anterior blepharitis in Misurata region, Libya. Dentistry and Medical Research, 2, 8–13. Scholar
  89. Nikolaev, Y. A., & Plakunov, V. K. (2007). Biofilm—“City of microbes” or an analogue of multicellular organisms? Microbiology, 76, 125–138. Scholar
  90. Nordmann, P., Poirel, L., Walsh, T. R., & Livermore, D. M. (2011). The emerging NDM carbapenemases. Trends in Microbiology, 19, 588–595. Scholar
  91. Okajima, Y., Kobayakawa, S., Tsuji, A., & Tochikubo, T. (2006). Biofilm formation by Staphylococcus epidermidis on intraocular Lens material. Investigative Ophthalmology and Visual Science, 47, 2971–2975. Scholar
  92. Olatunji, F. O., Fadeyi, A., Ayanniyi, A. A., & Akanbi, A. A. (2007). Non-gonococcal bacterial agents of conjunctivitis and their antibiotic susceptibility patterns in Ilorin, Nigeria. African Journal of Medicine and Medical Sciences, 36, 243–247.PubMedGoogle Scholar
  93. Ozkan, J., Zhu, H., Gabriel, M., et al. (2012). Effect of prophylactic antibiotic drops on ocular microbiota and physiology during silicone hydrogel Lens Wear. Optometry and Vision Science, 89, 326–335. Scholar
  94. Pathengay, A., Mathai, A., Shah, G. Y., & Ambatipudi, S. (2010). Intravitreal piperacillin/tazobactam in the management of multidrug-resistant Pseudomonas aeruginosa endophthalmitis. Journal of Cataract and Refractive Surgery, 36, 2210–2211. Scholar
  95. Perkins, R. E., Kundsin, R. B., Pratt, M. V., et al. (1975). Bacteriology of normal and infected conjunctiva. Journal of Clinical Microbiology, 1, 147–149.PubMedPubMedCentralGoogle Scholar
  96. Pierre, D. J., & Tang, J. (2010). Bleb associated endophthalmitis with methicillin-resistant Staphylococcus aureus. The British Journal of Ophthalmology, 94, 390–392. Scholar
  97. Rahman, Z. A., Harun, A., Hasan, H., et al. (2013). Ocular surface infections in northeastern state of malaysia: A 10-year review of bacterial isolates and antimicrobial susceptibility. Eye and Contact Lens, 39, 355–360. Scholar
  98. Ramachandran, L., Sharma, S., Sankaridurg, P. R., et al. (1995). Examination of the conjunctival microbiota after 8 hours of eye closure. The CLAO Journal, 21, 195–199.PubMedGoogle Scholar
  99. Reddy, A. K., Garg, P., Babu, K. H., et al. (2010). In vitro antibiotic susceptibility of rapidly growing nontuberculous mycobacteria isolated from patients with microbial keratitis. Current Eye Research, 35, 225–229. Scholar
  100. Rogers, B. A., Aminzadeh, Z., Hayashi, Y., & Paterson, D. L. (2011). Country-to-country transfer of patients and the risk of multi-resistant bacterial infection. Clinical Infectious Diseases, 53, 49–56. Scholar
  101. Sadaka, A., Durand, M. L., Sisk, R., & Gilmore, M. S. (2017). Staphylococcus aureus and its bearing on ophthalmic disease. Ocular Immunology and Inflammation, 25, 111–121. Scholar
  102. Sanfilippo, C. M., Hesje, C. K., Haas, W., & Morris, T. W. (2011). Topoisomerase mutations that are associated with high-level resistance to earlier fluoroquinolones in Staphylococcus aureus have less effect on the antibacterial activity of Besifloxacin. Chemotherapy, 57, 363–371. Scholar
  103. Sanfilippo, C. M., Morrissey, I., Janes, R., & Morris, T. W. (2016). Surveillance of the activity of aminoglycosides and fluoroquinolones against ophthalmic pathogens from Europe in 2010–2011. Current Eye Research, 41, 581–589. Scholar
  104. Schachter, B. (2003). Slimy business—The biotechnology of biofilms. Nature Biotechnology, 21, 361–365. Scholar
  105. Schimel, A. M., Miller, D., & Flynn, H. W. (2013). Endophthalmitis isolates and antibiotic susceptibilities: A 10-year review of culture-proven cases. American Journal of Ophthalmology, 156, 50–52.e1. Scholar
  106. Senok, A. C., Botta, G. A., & Soge, O. O. (2012). Emergence and spread of antimicrobial-resistant pathogens in an era of globalization. Interdisciplinary perspectives on infectious diseases, 2012, 1–3. Scholar
  107. Sharma, A. (2011a). Antimicrobial resistance: No action today, no cure tomorrow. Indian Journal of Medical Microbiology, 29, 91–92. Scholar
  108. Sharma, S. (2011b). Antibiotic resistance in ocular bacterial pathogens. Indian Journal of Medical Microbiology, 29, 218–222. Scholar
  109. Sherwal, B., & Ak, V. (2008). Epidemiology of ocular infection due to bacteria and fungus – a prospective study. JK Science, 10, 127–131.Google Scholar
  110. Shiferaw, T., Beyene, G., Kassa, T., & Sewunet, T. (2013). Bacterial contamination, bacterial profile and antimicrobial susceptibility pattern of isolates from stethoscopes at Jimma University specialized hospital. Annals of Clinical Microbiology and Antimicrobials, 12, 39. Scholar
  111. Shimizu, K., Kobayakawa, S., Tsuji, A., & Tochikubo, T. (2006). Biofilm formation on hydrophilic intraocular Lens material. Current Eye Research, 31, 989–997. Scholar
  112. Shimizu, Y., Toshida, H., Honda, R., et al. (2013). Prevalence of drug resistance and culture-positive rate among microorganisms isolated from patients with ocular infections over a 4-year period. Clinical Ophthalmology, 7, 695–702. Scholar
  113. Shin, H., Price, K., Albert, L., et al. (2016). Changes in the eye microbiota associated with contact Lens wearing. MBio, 7, e00198–e00116. Scholar
  114. Shirodkar, A. R., Pathengay, A., Flynn, H. W., et al. (2012). Delayed- versus acute-onset Endophthalmitis after cataract surgery. American Journal of Ophthalmology, 153, 391–398.e2. Scholar
  115. Sridhar, M. S., Sharma, S., Garg, P., & Rao, G. N. (2001). Treatment and outcome of nocardia keratitis. Cornea, 20, 458–462.CrossRefGoogle Scholar
  116. Stapleton, F., Willcox, M., Sansey, N., & Holden, B. (1997). Ocular microbiota and polymorphonuclear leucocyte recruitment during overnight contact lens wear. Australian and New Zealand Journal of Ophthalmology, 25, 33–35. Scholar
  117. Stewart, P. S., & Franklin, M. J. (2008). Physiological heterogeneity in biofilms. Nature Reviews. Microbiology, 6, 199–210. Scholar
  118. Suzuki, T., Kawamura, Y., Uno, T., et al. (2005). Prevalence of Staphylococcus epidermidis strains with biofilm-forming ability in isolates from conjunctiva and facial skin. American Journal of Ophthalmology, 140, 844–850.e1. Scholar
  119. Tuft, S. J. (2000). In vitro antibiotic resistance in bacterial keratitis in London. The British Journal of Ophthalmology, 84, 687–691. Scholar
  120. Ubani, U. (2009). Common bacterial isolates from infected eyes. Journal of the Nigerian Optometric Association, 15, 40–47. Scholar
  121. Uhlén, M., Guss, B., Nilsson, B., et al. (1984). Complete sequence of the staphylococcal gene encoding protein A. A gene evolved through multiple duplications. The Journal of Biological Chemistry, 259, 1695–1702.PubMedGoogle Scholar
  122. Vafidis, G. C., Marsh, R. J., & Stacey, A. R. (1984). Bacterial contamination of intraocular lens surgery. The British Journal of Ophthalmology, 68, 520–523. Scholar
  123. Walter, J., Noll, I., Feig, M., et al. (2017). Decline in the proportion of methicillin resistance among Staphylococcus aureus isolates from non-invasive samples and in outpatient settings, and changes in the co-resistance profiles: An analysis of data collected within the antimicrobial resistance Sur. BMC Infectious Diseases, 17, 169. Scholar
  124. Willcox, M. D. P. (2013). Characterization of the normal microbiota of the ocular surface. Experimental Eye Research, 117, 99–105. Scholar
  125. Yong, D., Toleman, M. A., Giske, C. G., et al. (2009). Characterization of a new Metallo- -lactamase gene, blaNDM-1, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrobial Agents and Chemotherapy, 53, 5046–5054. Scholar
  126. Zhang, K., McClure, J.-A., Elsayed, S., & Conly, J. M. (2009). Novel staphylococcal cassette chromosome mec type, tentatively designated type VIII, harboring class A mec and type 4 ccr gene complexes in a Canadian epidemic strain of methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 53, 531–540. Scholar
  127. Zhou, Y., Holland, M. J., Makalo, P., et al. (2014). The conjunctival microbiome in health and trachomatous disease: A case control study. Genome Medicine, 6, 99. Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Sarim Ahmad
    • 1
  • Shamim Ahmad
    • 2
  • Faizan Abul Qais
    • 3
  • Mohammad Shavez Khan
    • 3
  • Iqbal Ahmad
    • 3
  1. 1.Department of Oral pathology and Microbiology, Santosh Dental CollegeSantosh UniversityGhaziabadIndia
  2. 2.Division of Microbiology, Institute of Ophthalmology, JN Medical CollageAligarh Muslim UniversityAligarhIndia
  3. 3.Department of Agricultural Microbiology, Faculty of Agricultural SciencesAligarh Muslim UniversityAligarhIndia

Personalised recommendations