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 Table of Contents  
REVIEW ARTICLE
Year : 2017  |  Volume : 55  |  Issue : 4  |  Page : 293-297

Lacrimal sac infections and microbial analysis


Dr. Agarwal's Eye Hospital and Eye Research Centre, Chennai, Tamil Nadu, India

Date of Web Publication25-Apr-2018

Correspondence Address:
Dr. Dhivya Ashok Kumar
Dr. Agarwal's Eye Hospital and Eye Research Centre, 19, Cathedral Road, Chennai - 600 086, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/tjosr.tjosr_23_18

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  Abstract 


Lacrimal sac infection is one of the common pathologies in a routine ophthalmic practice. Dacryocystitis often present as epiphora with or without discharge. Regurgitation of mucopurulent discharge from punctum is a specific indicator of sac infection. In this article, we have reviewed the literature on the microbial spectrum in lacrimal duct obstruction with sac infection. The common microbial organism and the antibiotic sensitivity status of the same have also been reviewed. More than 90% culture positivity is noted in all the studies as noted in the literature. Gram-positive organism is the commonest source of infection. Staphylococcal species, namely, Staphylococcus aureus have been noted to be the most common among the Gram-positive organisms. The other Gram-positive organisms include Streptococcus pneumonia and Staphylococcus epidermidis. The Gram-negative organisms predominantly seen are Pseudomonas aeruginosa, Hemophilus influenza, and Klebsiella. Very rarely anaerobic organism such as Propionibacterium, fungi like Candida, other Gram-negative microbes such as Enterobacter, and occasionally, Mycobacterium are also cultured. Gram-positive organisms are sensitive to Vancomycin, Ofloxacin, Gatifloxacin, and Chloramphenicol. Gram-negative organisms showed sensitivity to Tobramycin. Resistant to topical quinolones has also been reported in some studies. The overall antibiotic sensitivity has been good and encouraging in the management of lacrimal sac infections.

Keywords: Bacteriology of lacrimal sac, dacrocystitis, dacrocystorhinostomy, lacrimal sac, microbial analysis of lacrimal sac


How to cite this article:
Kumar DA. Lacrimal sac infections and microbial analysis. TNOA J Ophthalmic Sci Res 2017;55:293-7

How to cite this URL:
Kumar DA. Lacrimal sac infections and microbial analysis. TNOA J Ophthalmic Sci Res [serial online] 2017 [cited 2019 Jul 17];55:293-7. Available from: http://www.tnoajosr.com/text.asp?2017/55/4/293/231123




  Introduction Top


Every ophthalmic surgeon would have faced the patients with the lacrimal sac pathologies in his or her routine ophthalmic out patient service. Dacryocystitis, the infection of the lacrimal sac is one of the common conditions encountered in the lacrimal system diseases. Acute dacryocystitis is often presents as an acute eye pain, periocular swelling, and fever. Chronic dacryocystitis is often diagnosed with the persistent epiphora with or without regurgitation of the mucoid or mucopurulent material on pressure over the sac area, or regurgitation of mucoid or mucopurulent discharge on irrigation of the lacrimal drainage system. The mucopurulent discharge from lacrimal punctum or the underlying conjunctiva has been the source of the specimen for microbial analysis in the large scale. There have been wide ranges of bacteriological analysis studies of swab cultures from the conjunctiva, the lacrimal sac, and the sac biopsy specimen from worldwide. In this review article, the spectrum of the microbial growth in the lacrimal sac and the changes in drug sensitivity and resistance have been presented.


  Materials and Methods Top


A meta-analysis and review of the literature on the existing studies and research on the human lacrimal sac microbial spectrum and drug sensitivity and resistance have been performed. Search engines such as PubMed, Google, and science direct were utilized for the sources of the literatures search. Individual theses of the postgraduate students were also analyzed.


  Anatomical Considerations Top


Lacrimal sac

The lacrimal sac is located within the lacrimal fossa, which is bound anteriorly by the frontal process of the maxillary bone (anterior lacrimal crest) and posteriorly by the lacrimal bone (posterior lacrimal crest). Differing proportions of the lacrimal bone and the maxillary bone make up the lacrimal fossa; the position of the vertically oriented suture between them is variable. The thickness of the lacrimal bone varies; however, the lacrimal bone is generally thinner than the maxillary bone. The lacrimal bone can be localized intranasally by its position, which is anterior to the uncinate process of the ethmoid bone. The lacrimal sac is lined by a double-layered epithelium (superficial is columnar and deep is flatter). It can be divided into a fundus superiorly and a body inferiorly. The fundus extends 3 mm–5 mm above the superior portion of the medial canthal tendon, and the body extends approximately 10 mm below the fundus to the osseous opening of the nasolacrimal canal. At the posterior lacrimal crest, the orbital periosteum splits into envelop the lacrimal sac as a covering known as the lacrimal fascia. This periosteum then continues inferiorly to enclose the nasolacrimal duct (NLD). The lacrimal fascia is surrounded by the fibers of the orbicularis oculi muscle, the superficial head of the muscle travels around the front of the sac to attach to the anterior lacrimal crest, and the deep head of the muscle travels behind the sac to attach to the posterior lacrimal crest. Between the lacrimal fascia and the lacrimal sac lies a venous plexus. Lacrimal sac mucosa has a variety of anti-infection strategies to prevent the colonization by microorganisms. The first line of defense against invading pathogens is the lacrimal sac epithelium, where the cells are tightly bound together to protect the underlying tissues from the viral or bacterial invasion.[1],[2] The epithelial cells also secrete immunoglobulin A, anti-infection peptides, and mucins. The lacrimal drainage-associated lymphoid tissue (LDALT) integrated with the activities of the epithelium, forms the second line of defense.[3] The LDALT is primarily a part of the mucosa-associated lymphoid tissue. These defense mechanisms prevent attacks from the bacteria that could lead to dacryocystitis.

Nasolacrimal duct

The lacrimal sac continues downwards as the NLD. NLD consists of a 12-mm superior intraosseous portion and a 5-mm inferior membranous portion. The bony nasolacrimal canal is approximately 1 mm in diameter; the intraosseous part travels posterolaterally through the nasolacrimal canal within the maxillary bone, while the membranous part runs within the nasal mucosa, eventually opening into the inferior meatus under the inferior nasal turbinate. The valve of Hasner is present at the opening of the NLD within the nasal cavity. NLD is also lined by the double layer of the epithelium the same double layer of the epithelium similar to the sac. The mucin of the epithelium together with the trefoil factor family peptides influence the rheological properties of tear fluid and have antimicrobial defense and enhance the tear transport.[4]


  Microbiology Top


A clinico-bacteriological study of chronic dacryocystitis in adults revealed the positivity for the bacterial growth in only 53.6% of their samples in India.[5] Gram-positive organisms were the most common isolates. Staphylococcus aureus (40.0%) was found to be the most common Gram-positive organism, followed by Staphylococcus epidermidis (10.0%) and Streptococcus pneumoniae (10.0%). Among the Gram-negative organisms, Pseudomonas aeruginosa (16.6%) was the most common. This study revealed that chronic dacryocystitis is more common in females and the left eye is more frequently involved than the right eye. It is common among the lower socioeconomic strata with the habit of pond bathing. Some forms of the nasal pathology such as hypertrophied inferior turbinate, deviated nasal septum, nasal polyp, and allergic rhinitis were found in 19.6% of the patients. Complications of the chronic dacryocystitis such as conjunctivitis, corneal ulcer, acute on chronic dacryocystitis, lacrimal abscess, and fistula were seen in 25% of these patients; about 53.6% of the culture samples were positive for the bacterial growth. Das et al. from the North-Eastern India found 494 samples (90.97%) positive for bacteria, including both single and mixed isolations.[6] The majority of microorganisms in their study was Gram-positive bacteria. Nearly 75% of the overall microorganisms cultured were Gram-positive bacteria, with a predominance of Staphylococcus species. Gram-negative bacteria were isolated in 25% of the specimens with a predominance of P. aeruginosa. A clinico-bacteriological study of the chronic dacryocystitis in Southern India found the coagulase-negative Staphylococci and S. aureus to be the most common isolates (71% and 14%, respectively).[7] Bharathi et al. in a large study from Tamil Nadu found coagulase-negative Staphylococci (44.2%), S. aureus (10.8%), and S. pneumonia (10%) as the causative organisms for the chronic dacryocystitis.[8]

A comparative bacteriological profile and antibiogram of dacryocystitis study in Nepal population showed an equal distribution of both Gram-positive and negative bacterial isolates.[9] However, Badhu el al. from Nepal reported S. pneumonia as the most frequently isolated organism.[10] The prevalence of bacterial pathogens responsible for the chronic dacryocystitis were coagulase-negative Staphylococci (52.2%) and Klebsiella pneumonia (17.4%), as reported in an Egyptian study.[11] This report is in contrast to other similar studies. Sainju et al. have reported the predominance of S. aureus (34.2%) in dacryocystitis among the Southern Australian population.[12] Sun et al. have studied the microbiology of the chronic dacryocystitis in China and reported that Staphylococcus species constituted 34.5% of isolates in their series.[13] In an Iranian study, the prevalence of Gram-positive, Gram-negative, and culture-negative samples were 77.4%, 18.9%, and 3.8%, respectively, in the chronic dacryocystitis, with Staphylococcus epidermis being the most common organism.[14] In the lacrimal duct, oxygen was consumed by the growth and the propagation of aerobic and facultative bacteria. This may provide anaerobic conditions for the growth of anaerobic bacteria and cause the pathological changes by anaerobes such as Propionibacterium. Previously, anaerobic bacteria have been reported to account for 7% of isolates.[15] Briscoe et al. showed the most common isolates as Pseudomonas (22%), S. aureus (13%), Enterobacter (10%), Citrobacter (10%), S. pneumoniae,  Escherichia More Details coli, and Enterococcus (7%) in their series.[16] Uncommon Gram-negative bacteria were also cultured: Alcaligenes in two cases (5%) and one case of Stenotrophomonas maltophilia (2.5%). A higher incidence of Gram-negative organisms, particularly Pseudomonas with resistance to the commonly used antibiotics was found in this study.

An US-based multicentered prospective study has reported to have done the microbial analysis of dacryocystitis which was performed in 16 centers and compared the acute with the chronic group of infections.[17] Of all 89 patients, there were 80 total culture isolates with 55 (68.8%) Gram-positive isolates, 23 (28.7%) Gram-negative isolates, and 2 (2.5%) Mycobacterium isolates. In the acute group, 78.3% were Gram-positive and 21.7% were Gram-negative. In the chronic group, 64.9% were Gram-positive, 31.6% were Gram-negative, and 3.5% were Mycobacterium isolates. The proportions of Gram-positive and Gram-negative organisms between groups revealed no statistically significant difference.

In congenital NLD obstruction, Kuchar et al. have reported that cultures were positive for bacteria from 72.64% of the samples, where 73 isolates were recovered from the 50 samples.[18] The spectrum was S. pneumoniae, representing 35.4% of the isolates, followed by Haemophilus influenza (19.6%). Usha et al. evaluated 238 samples with a clinical diagnosis of congenital NLD obstruction, 197 (83%) yielded a positive culture. Gram-positive organisms contributed 124 (57%) with S. Pneumoniae being the common growth and Gram-negative was 93(47%) and Haemophilus influenza was the frequent isolate in Gram-negative category.[19] One case of the fungal isolate (0.5%) of Candida tropicalis was also reported by them. The age of onset is usually in the neonatal period with a female preponderance.[20] The clinical spectrum ranges from classic pediatric acute dacryocystitis to meningitis. S. aureus is the most common isolate. Occasionally acquired etiologies and rare organisms such as Pantoea sp., Epstein-Barr Virus, and Sporothrix are implicated in the etiopathogenesis.[20]

Microbiological assessment

For all practical purposes, the bacteriological samples can be obtained from the conjunctival sac, the lacrimal sac, and also from the intraoperative lacrimal sac material.[6],[7],[8],[17],[21] It is important that all surgeons should know the basic methodology of processing of the material obtained. The collection of the samples were performed by either applying pressure over the lacrimal sac region and allowing the purulent material to reflux through the lacrimal punctum, or by irrigating the lacrimal drainage system with sterile saline and collecting the sample from the refluxing material. The samples were collected with sterile cotton wool swabs, ensuring that the lid margin or the conjunctiva was not touched. The specimen material obtained is initially inoculated directly on the surface of the solid media as sheep's blood agar, chocolate agar, and Sabouraud's dextrose agar and also inoculated into the depth of the liquid media as brain heart infusion agar and thioglycollate medium. The material obtained is also smeared onto a clean, sterile labeled glass slides for 10% potassium hydroxide wet mount, Gram-stain, and Ziehl-Neelsen acid-fast stain. All inoculated media are incubated aerobically. The inoculated Sabouraud's dextrose agar was incubated at 27°C, examined daily, and discarded at 3 weeks if no growth is seen. The inoculated blood agar, chocolate agar, thioglycollate broth, brain heart infusion agar are incubated at 37°C, examined daily, and discarded at 7 days if growth is not seen. The microbial cultures should be considered significant, (1) if the growth of the same organism is revealed on more than one solid-phase medium, (2) if there is confluent growth at the site of inoculation on one solid medium, (3) if growth of one medium is consistent with direct microscopy findings (i.e., appropriate staining and morphology with Gram-stain), and/or (4) if the same organism is grown from >1 specimen.[22],[23],[24]

The specific identification of bacterial isolates should be performed based on the microscopic morphology, staining characteristics, and biochemical properties using the standard laboratory criteria.[25] Standardized bacterial inoculum for the susceptibility testing has to be prepared as per the standardized methods.[26],[27] When blood agar was tested, the susceptibility is measured by measuring the area where hemolysis did not occur.[26],[27] The zone diameter for an individual antimicrobial agent should be translated into the sensitivity and resistant categories by referring to an interpretative chart as per the recommendation of the National Committee for Clinical Laboratory Standards, Villanova, PA, USA.

Sensitivity and resistance

Antibiotic use for dacryocystitis is widely practiced in our part of the world. In the study by Mandal et al., Chloramphenicol was effective against most of the Gram-positive organisms. Aminoglycosides, Tobramycin, in particular, was effective against S. epidermidis. Fluoroquinolones, namely, ciprofloxacin and ofloxacin were effective against P. aeruginosa and K. pneumoniae.[5] Chaudhry et al. have reported a 97.3% of culture positivity in dacryocystitis in adults in a population which included 188 eyes.[28] The high rate of microorganism-positive lacrimal sac cultures suggests that adult patients should be treated for their infection before any intraocular surgery due to the potential risk of infection. The analysis of thein vitro susceptibility by Amin et al.[21] showed that the highest percentage of bacterial isolates was most susceptible to vancomycin (95.1%), gatifloxacin (91.8%), Cefotaxime (91.8%), and Amikacin (91.1%), Tobramycin (88.5%), and Ofloxacin (88.5%), while the highest percentage of bacterial isolates were resistant to macrolides (42.3%) and amoxicillin (37.7%). They also found that, of all antibacterial agents tested, gatifloxacin and ofloxacin showed the lowest percentage of resistance to all categories of bacterial species recovered from both acute and chronic infections of the lacrimal apparatus (8.2% and 11.5%, respectively). The analysis of the resistance pattern by Amin et al.[21] showed a variation in the resistance of isolates recovered from an acute and chronic dacryocystitis. The percentage of resistance of bacterial isolates recovered from chronic infections to Tobramycin (5 of 35; 14.3%), Gatifloxacin (5 of 35; 14.3%), Ciprofloxacin (8 of 35; 22.9%), Ofloxacin (7 of 35; 20%), and Amoxicillin clavulinate (8 of 35; 22.9%) was found to be higher than the percentage of resistance of bacterial isolates recovered from an acute infection to Tobramycin (12.5% 2 of 16), Gatifloxacin (0), Ciprofloxacin (0), Ofloxacin (0), and amoxicillin clavulanate (3 of 16 18.75%). Pornpanich et al. reported that antimicrobial susceptibility testing revealed that ciprofloxacin was the most effective drug against all Gram-positive and Gram-negative organisms.[29]

In the report by Mills et al., the frequency of methicillin-resistant S. aureus in the acute group, 4/23 (17.4%), was greater than the chronic group, 1/57 (1.8%) (P ≤ 0.01).[17] The sensitivity testing revealed an ofloxacin and tetracycline to be the most effective drugs as monotherapy. Clinically, the combination of bacitracin and neomycin, primarily used in half of the patients as initial therapy, was successful in curing the dacryocystitis in 82.5% of all patients.[19] The drug sensitivity in their report showed that the Gram-positive bacteria were sensitive to chloramphenicol, vancomycin, and ofloxacin and Gram-negative bacteria were sensitive to ofloxacin and ciprofloxacin.

Compared to other developing countries, India has a high rate of antibiotic use. Inappropriate use of topical antibiotics can clearly cause the risk of developing bacterial resistance among bacterial flora in lacrimal apparatus. The use of broad-spectrum antibiotics is another risk factor for developing bacterial resistant, and therefore, utmost care has to be taken while administration of antimicrobials. The diagnosis of dacryocystitis is usually clinically aided by the laboratory investigations. There has been a change in the spectrum of organisms, where S. pneumoniae has reduced and later Staphylococcus became common.[30] In the recent decades, S. aureus has become predominant. The emergence of rare species, highly resistant microbes, and Gram-negative microorganisms may also indicate a changing trend in the lacrimal sac infections.


  Conclusion Top


Bacterial colonization occurs regularly in the obstructed NLD and leads to infection in the majority of patients. Gram-positive organisms are often predominantly observed followed by Gram-negative organisms. All widely used antibiotics are usually effective in the management of dacryocystitis. However, proper care has to be taken in prescribing and treating these sac infections, which can sometimes be vision threatening due to its associated sequelae or complications. Nevertheless, better antibiotics, well-established laboratory techniques, surgical modalities, and improved patient care logistics have contributed to good outcomes in the lacrimal sac infections in the past few decades.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Sun X, Liang Q, Luo S, Wang Z, Li R, Jin X, et al. Microbiological analysis of chronic dacryocystitis. Ophthalmic Physiol Opt 2005;25:261-3.  Back to cited text no. 13
    
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Razavi ME, Ansari-Astaneh MR, Farzadnia M, Rahmaniyan H, Moghiman T. Bacteriological evaluation of adult dacryocystitis in Iran. Orbit 2010;29:286-90.  Back to cited text no. 14
    
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Briscoe D, Rubowitz A, Assia EI. Changing bacterial isolates and antibiotic sensitivities of purulent dacryocystitis. Orbit 2005;24:95-8.  Back to cited text no. 16
    
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