Anaerobic Bacteria
Rebecca L. Penland
Michael S. Osato
Kirk R. Wilhelmus
The eye and ocular adnexa are prone to colonization by anaerobic bacteria that are also part of the flora of periorbital skin, paranasal sinuses, and the oral cavity. Once thought harmless commensals, anaerobes are now implicated in many human eye infections. Advances in microbiologic techniques enable the recovery and identification of obligately anaerobic bacteria from clinical specimens.
The prevalence and incidence of anaerobic infections remain unknown because of variations in culture technique and in criteria used to assess infection. Strict methodologic procedures are required to prevent exposure of anaerobes to atmospheric oxygen. Fortunately, most pathogenic anaerobes are relatively aerotolerant and may survive in culture despite periods of oxygen exposure.
Extensive tissue necrosis, gas in tissue, and foul-smelling discharge are clues to anaerobic infections of soft tissues, but clinical signs of anaerobic ocular infection usually are nonspecific. Some cases of anaerobic ocular infection probably are missed because appropriate laboratory studies are not performed. Many ocular infections involve aerobic, facultative, and anaerobic organisms,1,2 especially when bacteria originate from the patient’s indigenous microflora. The polymicrobial composition of anaerobic infections complicates the interpretation of laboratory findings, especially in the presence of other known highly pathogenic microorganisms.
BACTERIOLOGY
Anaerobes reported to infect the human eye are listed in Table 1. The taxonomy and classification of anaerobic bacteria continue to undergo revision. The genus Bacteroides now includes the bile-resistant species that were included previously in the B. fragilis group. Saccharolytic species that were formerly in the genus Bacteroides are now included in the genus Prevotella, whereas asaccharolytic or weakly saccharolytic species are now classified as Porphyromonas. Both genera include pigmented and nonpigmented species.3
TABLE ONE. Anaerobic Bacteria of Ocular Importance | ||||||||||||||||||||||||
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The genus Peptococcus now contains only one species, P. niger, which is rarely recovered from clinical specimens. Several species from the genus Peptococcus were transferred to the genus Peptostreptococcus when DNA analysis revealed similar G+ C content. Peptostreptococci appear to be closely related to Clostridium. Arachnia propionica, an anaerobic gram-positive nonspore-forming rod, has been reclassified as Propionibacterium propionicum.4
NORMAL ANAEROBIC BACTERIAL FLORA OF THE EXTERNAL EYE
Clinical studies have shown that anaerobic bacteria are isolated readily from the external ocular structures of healthy individuals. Up to 80% of normal adults harbor anaerobes in their conjunctival sac or on their lid margins.5,6,7,8 The relative distribution and composition of the anaerobic bacterial flora of the external eye vary with the geographic location of the study, the population examined, and the age of the individuals.8
Propionibacterium acnes is one of the predominant organisms residing on the ocular surface and has been isolated from approximately 50% of normal eyes.5,6,7 P. acnes may enter the eye during cataract and other intraocular surgical procedures and has been found to persist inside the eye for up to 3 years.9,10 Other propionibacteria (P. avidum and P. granulosum), P. niger, peptostreptococci, and occasionally Bacteroides species also are indigenous to the external ocular surfaces.5,6,7,11 The frequency of Bacteroides may be lower than that suggested by the ophthalmic literature since many studies were performed before the reclassification of several Bacteroides species as Prevotella or Porphyromonas.
Immune status, antiobiotic exposure, and environment contribute to anaerobic colonization of the conjunctivae. In a study comparing the conjunctival flora of human immunodeficiency virus (HIV)-infected patients and healthy individuals, a slightly higher percentage of cultures from patients with acquired immunodeficiency syndrome (AIDS) yielded anaerobes.12 Different organisms were recovered from persons with AIDS, including Actinomyces and several species of Clostridium. However, all patients with AIDS were hospitalized for secondary infections at the time of the study, and antimicrobial treatment probably was an important factor in the altered anaerobic flora.
PREDISPOSING FACTORS
Any ocular structure is vulnerable to anaerobic bacterial infection. The exogenous route of infection is most common, whether from contaminants associated with accidental injury or from organisms of the normal ocular flora. Blood-borne endogenous ocular infection is uncommon but has occurred. Spread from adjacent structures to the eye and ocular adnexa is rare but may be involved in some cases of orbital disease associated with sinusitis.
Systemic anaerobic infections and infections of the eye and ocular adnexa share common features with regard to predisposition to infection. Vascular injury, compression, and tissue edema from trauma, elective surgery, or infection with aerobic or facultative bacteria are the primary factors predisposing to anaerobic infection (Table 2). These processes favor the growth of anaerobic bacteria by decreasing vascular permeability, lowering the local redox potential, and providing a portal of entry for these relatively noninvasive bacteria.13,14
TABLE TWO. Predisposing Factors to Anaerobic Ocular Infection | |
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Altered structure of ocular tissues by previous infection or underlying illness (e.g., malignancy, diabetes mellitus, or Sjögren’s syndrome) can decrease the host’s resistance to infection. The use of corticosteroids or antibiotics can predispose to anaerobic infection by impairing the normal inflammatory and immune responses.
The role of biofilm on contact lenses, intraocular lenses, and other biomaterials also may play a role in anaerobic ocular infection. In one series of contact lens-related keratitis, one third of confirmed anaerobic ocular infections was associated with soft contact lens wear.15
PATHOGENESIS
Anaerobic bacteria produce several virulence factors that contribute to the pathogenesis of infection. Structures mediating attachment and adhesion, the production of hydrolytic enzymes and proteases, and the ability to evade the immune system are important virulence factors.16 In addition to various predisposing host factors, other important aspects of pathogenesis are the polymicrobial nature of most anaerobic infections and the resulting synergistic interactions among multiple bacterial species.
GRAM-POSITIVE ANAEROBES
Anaerobic cocci occasionally are isolated from ocular infections.17 Peptostreptococci are causes of keratitis18 and endophthalmitis. Although these bacteria, as a group, are metabolically inactive in vitro,19 enzyme production and capsule formation are variable. The production of gelatinase, collagenase, and hyaluronidase by some species of Peptostreptococcus has been reported.20
Clostridium perfringens can cause conjunctivitis,21 eyelid and orbital infections,22 necrotizing keratitis,23 and panophthalmitis in humans.24,25,26,27 Intraocular infection is fulminant, with retinal necrosis and destruction. Other clostridial species (e.g., C. bifermentans and C. septicum) also have been rarely encountered.28,29 Clostridial ocular infections have occurred in dogs, horses, and other animals.30 The only extracellular enzyme directly associated with invasive anaerobic infection is the α-toxin (phospholipase C) of C. perfringens.31,32 Other toxins include collagenase33 and hyaluronidase.
P. acnes is the anaerobe isolated most frequently from ocular infections.6,34,35 Although this anaerobe releases a chemoattractant for leukocytes, P. acnes resists killing by neutrophils, inhibits the generation of specific suppressor T cells, and can persist within macrophages. P. acnes also can act as a nonspecific stimulator of the immune system.
P. acnes is implicated in several forms of ocular infection, ranging from chronic inflammation to acute suppuration and necrosis. P. acnes may contribute to the pathogenesis of rosacea and other forms of Meibomian gland dysfunction and blepharitis. P. acnes also has been isolated from rare cases of acute suppurative keratitis.36 Corneal infection due to this anaerobe has occurred in association with contact lens wear, corneal trauma, recurrent corneal erosion, herpetic keratitis, and other predisposing conditions.
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