ETIOLOGY

The anaerobic bacteria are a large and taxonomically diverse group of bacteria that are unable to survive in the presence of free oxygen concentrations greater than about 5 μM.² Sensitivity to molecular oxygen results from their inability to detoxify reactive oxygen molecules formed as a byproduct of either respiratory metabolism or exposure to ambient levels of atmospheric oxygen. Bacteria that are tolerant of oxygen or that utilize oxygen metabolically (obligate aerobes and facultative anaerobes) typically possess enzymes such as catalase, superoxide dismutase, and peroxidases to detoxify reactive oxygen molecules.³ These enzymes are generally absent in anaerobes because the detoxification reactions of catalase and dismutase result in formation of more molecular oxygen. To avoid the production of oxygen, the predominant metabolic pathways for obligately anaerobic bacteria are fermentative, and they utilize organic molecules as electron acceptors in energy production. The metabolic end products of carbohydrate and amino acid fermentation include volatile fatty acids, alcohols, indole, and sulfur compounds that are foul smelling, one of the hallmark clinical signs of anaerobic infections.⁴

Anaerobes have limited protection from exposure to oxygen by alternate detoxification pathways such as superoxide reductase. This enzyme produces hydrogen peroxide, which is detoxified into water by reductase and rubrerythrin pathways.^3,5 Aerotolerance is also quite variable among what are classified as obligate anaerobes, and growth of some obligate anaerobes such as Bacteroides may even be enhanced by low levels of oxygen (about 300 nM). Some obligate anaerobes may metabolically utilize, and detoxify, oxygen with cytochrome oxidase systems and oxygen-dependent respiratory chains.^2,3 These features may allow Bacteroides, as well as other obligate anaerobes with similar systems, to colonize mucous membranes or establish infections without prior colonization of and reduction of oxygen by facultatively anaerobic bacteria such as Escherichia coli.²

The taxonomy of anaerobic bacteria is complex and currently undergoing major revisions; this trend is likely to continue for the foreseeable future.^6–9 Although these taxonomic revisions are primarily of academic interest, they do reflect the difficulty in obtaining accurate identification of anaerobic isolates and may complicate the optimal selection of appropriate antimicrobial therapy. This also makes it difficult to compare the results of older studies to newer studies. The primary basis for this ongoing taxonomic reorganization is the use of nucleotide sequence-based phylogenetic analyses, particularly of the 16s ribosomal deoxyribonucleic acid (rDNA) gene, in place of the previously used, less reliable analyses based on phenotypic and biochemical characteristics.^7,9

For the aerobic and facultatively anaerobic bacteria, taxonomy based on phenotypic and biochemical characteristics correlate relatively well with genetic analyses. However, for anaerobes, schemes based on phenotypic and biochemical characteristics result in much greater discrepancies, including misclassification of organisms with regard to highly fundamental traits such as Gram-staining properties, morphology, aerotolerance, and spore formation.^6,7,9 Despite the dramatic changes in the classification of anaerobes and the great diversity of this group of bacteria, most of the clinically significant anaerobic pathogens of humans and other mammals, including horses, belong to a limited number of genera^7–16 (Table 48-1).

Table 48-1 Clinically Significant Obligately Anaerobic Bacteria of Humans, Horses, and Other Mammals

EPIDEMIOLOGY

Anaerobic bacteria are ubiquitous members of the normal flora of the skin and mucous membranes of all mammals,^7,12,17 and the major genera found as normal flora of horses appear to be similar to the clinically significant and normal flora anaerobes of humans and other mammals. It may seem somewhat counterintuitive that obligately anaerobic bacteria are found in high numbers at sites that are exposed to ambient air, such as the skin or oral cavity. However, in addition to the inherent aerotolerance that some obligate anaerobes possess, anaerobic microenvironments are created in these areas by the presence of facultatively anaerobic bacterial flora (including many of the other bacteria familiar to clinicians, such as staphylococci, streptococci, pasteurellas, actinobacilli, and members of the Enterobacteriaceae) that consume free oxygen.¹⁸ Anaerobes are also frequent opportunistic pathogens that cause infections when these bacteria gain access to anaerobic conditions in tissue, usually resulting from the presence of necrotic tissue and co-infection with facultatively anaerobic bacteria. Although anaerobes may cause infections by themselves, in most cases anaerobic infections are polymicrobic, with multiple obligately anaerobic bacteria as well as facultatively anaerobic bacteria.

Although most of the clinically significant anaerobes can be found on most sites of the body, certain genera are more common in certain sites. In humans the genera that predominantly colonize a given site are also those most likely to be found in infections associated with those anatomic areas, and detection of certain genera in the blood can predict the part of the body where the infection originates. Although this association has not been well demonstrated for horses, this most likely reflects the lack of information about normal equine anaerobic flora and routine anaerobic blood culturing rather than lack of such a correlation.

The most clinically important equine infections caused by obligately anaerobic bacteria are pneumonia and pleuropneumonia (see Chapter 1). Anaerobes that are reported from the equine oral and respiratory tracts include Bacteroides, Clostridium, Eubacterium, Fusobacterium, Peptostreptococcus, and Veillonella, as well a number of other, unidentified anaerobic gram-positive rods and cocci.^10,19,20 In one series of studies, 37% to 68% of lower respiratory tract infections had involvement of anaerobes, usually Bacteroides; 68% to 81% were mixed with facultative anaerobes such as streptococci, pasteurellas, actinobacilli, and Enterobacteriaceae; and 85% had multiple anaerobes.^14,15,21,22 The most frequently reported anaerobes from cases of equine respiratory disease include Bacteroides, Clostridium, Eubacterium, Fusobacterium, Peptostreptococcus, and Veillonella.^{10,14,15,20–27} The clinical significance of the anaerobic component of these infections is suggested by studies that found the presence of anaerobes was associated with decreased survival,^14,15,22,26 and horses treated with metronidazole showed improved clinical responses and survival rates.^15,24 The anaerobic bacteria involved in equine respiratory infections most likely arise from aspiration of normal oral flora, because most of the respiratory anaerobic pathogens are also found on the pharyngeal tonsillar surfaces.¹⁰ Anaerobes are also often associated with a variety of paraoral infections, including submandibular abscesses, mandibular osteomyelitis, sinus infection, and dental abscesses. The predominant anaerobes involved in these infections are very similar to those found in respiratory infections and as normal flora of pharyngeal tonsillar surfaces,¹⁰ and they presumably arise by extension from normal flora opportunistic infections.

Anaerobes are also common flora of the equine reproductive tract (see Chapter 8). In normal stallions, 96% of samples collected from the urethra, urethral fossa, smegma, and preejaculatory fluid contained Bacteroides, Clostridium, Fusobacterium, Peptococcus, and Peptostreptococcus. In normal mares, 100% of clitoral swabs, 24% of endometrial swabs, and 40% of endometrial washes contained Bacteroides, Clostridium, Fusobacterium, Peptococcus, and Peptostreptococcus spp.²⁸ Anaerobes, including Bacteroides, Clostridium, Fusobacterium

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