Atypical Wound Pathogens

Abstract

Background:

Atypical wound pathogens may be so described because they are uncommon pathogens of soft tissue among human beings, or because they may be fastidious and difficult to recover/isolate in the laboratory.

Methods:

A review of pertinent English-language literature was performed.

Results:

These wound pathogens are a diverse lot, including aerobic and anaerobic gram-positive and gram–negative bacilli, non-tuberculous mycobacteria, and bacteria that cannot be characterized conventionally because they lack a cell wall (the Mycoplasmataceae). They are diverse with respect to their virulence, but many are opportunistic pathogens.

Conclusions:

Among these atypical pathogens, clinical reports are most common of wound infections caused by Mycoplasma/Ureaplasma (sometimes as co-infecting agents), and the so-called rapidly growing non-tuberculous mycobacteria (Runyon Type IV; e.g., M. chelonae).

Surgical site infection (SSI) is well recognized but likely still under-reported, in large part because most operations, and thus most infections, occur in the ambulatory surgical setting where surveillance is rudimentary (to the extent that it exists at all) and reporting is voluntary and thus unreliable [1]. In the context of these shortcomings, the incidence of SSI is estimated to be approximately 3%. Most SSIs are superficial incisional SSIs (affecting only the skin and subcutaneous tissue) or deep incisional SSIs (affecting the fascia or muscle). Organ-space SSIs (e.g., intra-abdominal abscess, empyema thoracis) affect intra-cavitary spaces. If a SSI affects multiple tissue levels (e.g., an intra-abdominal abscess drains through an incision, causing infection at the level of the fascia), the infection should be classified according to the deepest manifestation [2].

The incidence of SSI is affected by a multiplicity of host and operative technical factors (summarized in the article by Fry [3]). High-risk patients include those with obesity, diabetes mellitus, immunosuppression, malnutrition, or a history of abuse of alcohol [4] or tobacco [5], among other factors. High-risk operations include those conducted in a “contaminated” (e.g., “spillage” from an inadvertent enterotomy during adhesiolysis for mechanical small bowel obstruction, operation within 12 h for a penetrating colon injury) or “dirty” field (i.e., operation to treat an established infection). Even some “clean” operations carry an increased risk of SSI (e.g., surgery of the breast [6], infra-inguinal arterial bypass grafting), whereas operations conducted in a “clean-contaminated” field (i.e., the planned opening of a aerodigestive or genitourinary hollow viscus) vary widely in risk. Among clean-contaminated operations, elective laparoscopic cholecystectomy in a healthy patient carries so little risk of SSI that routine antibiotic prophylaxis may be unwarranted [7], whereas elective surgery of the colon and rectum carries high risk [8], even when optimal pre-operative mechanical and oral antibiotic bowel preparation [9] is undertaken, regardless of the operative technique used.

In general, soft-tissue operations caudal to the inguinal ligament carry higher risk of SSI than those rostral to it, whereas the risk also increases as the incision carries deeper into a body cavity. Prolonged operations carry increased risk, especially if an agent with a short half-life (e.g., cefazolin, cefoxitin) is not re-dosed at an appropriate interval(s) intra-operatively [10].

There are scant data regarding some of the pathogens considered in this review. Therefore, for the purposes of this review, “wounds” of all types (e.g., traumatic wounds) will be considered.

Typical Microbiology

The predominant wound pathogens causing SSI depend greatly on the operation performed. Surgical site infections after clean operations limited to incision/dissection of skin and soft tissue (e.g., thyroid, breast, inguinal hernia) are caused predominantly by gram-positive cocci (e.g., Streptococcus spp., Staphylococcus spp., Enterococcus spp.) unless infra-inguinal, when SSI caused by aerobic or facultative gram-negative bacilli may be encountered. Clean-contaminated operations may be complicated by SSI caused by the aforementioned, or by gram-negative bacilli such as Escherichia coli or Klebsiella spp., among others (e.g., Enterobacteriaceae, Pseudomonas spp.). Anaerobic gram-positive cocci (e.g., Peptostreptococcus spp.) may cause infection after head and neck operations that enter the oral cavity or pharynx, whereas anaerobic gram-negative bacilli (e.g., Prevotella spp., Bacteroides spp., sometimes referred to as B. fragilis group) or anaerobic gram-positive bacilli (e.g., Clostridium spp.) may cause SSI after operation on any hollow viscus.

Most cases of SSI are mono-microbial, but mixed-pathogen infections are commonplace, especially after colon and rectal operations and surgical procedures of the head and neck. Some cases referred to previously as “culture-negative” infections [11] may in fact be because of anaerobes destroyed by exposure to oxygen as a result of haphazard specimen collection, or fastidious pathogens that are identifiable only by molecular diagnostics.

Atypical Wound Pathogens

By definition, SSIs caused by so-called atypical pathogens include none of the aforementioned microbes. Such infections are unusual and afflict mostly chronic wounds, although not exclusively. Predominantly opportunistic pathogens, the afflicted may be malnourished, immunosuppressed, or in the throes of a protracted hospitalization with exposure to multiple courses of broad-spectrum antimicrobial agents. The pathogens may have variable virulence expression, may be difficult to culture with standard microbiology laboratory techniques, and may not be identifiable unless molecular diagnostics are brought to bear. “Common” atypical wound pathogens are listed in Table 1.

Table 1.

Atypical Wound Pathogens

• Anaerobic bacteria

- Anaerococcus spp.

- Bacteroides spp. (see Table 3)

- Finegoldia magma

- Peptoniphilus spp.

• Gram-negative bacilli

- Aeromonas spp.

- Legionella spp.

- Vibrio spp.

• Gram-positive bacilli

- Actinomyces spp.

- Arcanobacterium spp.

- Corynebacterium spp.

• Aquatic bacteria

• Non-tuberculous mycobacteria

• “Rapidly-growing” mycobacteria (Runyon Type IV) (see Table 4.)

• Bacteria lacking a cell wall

- Mycoplasma spp.

- Ureaplasma spp.

Anaerobic gram-positive cocci

Anaerobic gram-positive cocci of clinical importance are found in three common genera (Peptostreptococcus, Gemella, and Streptococcus). Not all anaerobic cocci require stringent anaerobic conditions; for example, strains of S. intermedius are aerotolerant. Peptostreptococcus and Streptococcus are of the most clinical importance, with P. magnus the most frequent clinical isolate [12].

Peptoniphilus spp. are gram-positive anaerobic cocci that were classified formerly as Peptostreptococcus spp. [13]. There are seven species in the genus (P. asaccharolyticus, P. gorbachii, P. harei, P. ivorii, P. lacrimalis, and P. olsenii). The bacteria are part of normal resident vaginal and gut microbiota. They have been reported in numerous human infections besides SSI, including diabetic foot infections, bone/joint infections, blood stream infections, and chorioamnionitis. These organisms are difficult to recover with routine cultures. The 16S polymerase chain reaction (PCR) and matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) have facilitated identification of atypical pathogens generally [14].

Anaerococcus spp. are gram-positive anaerobic cocci [12], formerly classified variously as Micrococcus spp., Peptococcus spp., and Peptostreptococcus spp. There are eight species in the genus (A. senegalensis, A. murdochii, A. vaginalis, A. tetradius, A. prevotii, A. octavius, and A. lactolyticus), The bacteria are part of vaginal, skin, oropharyngeal, and gut microbiota. Anaerococcus spp. have been isolated from human infections, including abscesses (peritoneal, ovarian, lung) and diabetic foot infections, in addition to SSI.

Finegoldia magma is a gram-positive anaerobic coccus that was classified formerly as Peptostreptococcus magma. It is the only species in the genus. The bacterium is part of normal skin flora and colonizes mucous membranes. By contrast to several other anaerobic cocci, F. magma expresses several virulence factors. Biofilm formation is commonplace [12]. Finegoldia magma has been described as a pathogen in diabetic foot infections and decubitus ulcers. Notably, it may be clindamycin-resistant (Table 2).

Table 2.

Antimicrobial Susceptibilities of 43 Isolates of Finegoldia magma from the United Kingdom

Agent	Number (percent) resistant
Amoxicillin-clavulanic acid	0
Cefoxitin	0
Chloramphenicol	0
Clindamycin	3 ( 7)
Erythromycin	13 (30)
Imipenem-cilastatin	0
Metronidazole	0
Penicillin	0
Piperacillin-tazobactam	0
Tetracycline	16 (37)

Modified from Brazier et al. [13].

Aerobic gram-negative bacilli

Legionella spp. are thin, aerobic, pleomorphic, flagellated, non-spore–forming, gram-negative bacilli. Of the more than 70 species in the genus, L. pneumophilia, the etiologic agent of the respiratory infection Legionnaire disease, is most common and familiar. These are rare wound pathogens, usually in common with topical application of contaminated tap water [15]. In a report of 22 cases of extra-pulmonary legionellosis [16], most of the patients had undergone operations; 13 extra-pulmonary sites of infection were reported, including sinusitis, SSI after hip replacement, and prosthetic valve endocarditis.

Anaerobic gram-negative bacilli

The genus Bacteroides comprises at least 20 species known to cause clinical infection, although the exact number is a “moving target” because of molecular taxonomic classification techniques (as examples, B. distasonis, B. goldsteinii, and B. merdae have been re-classified into the Parabacteroides genus, whereas B. gracilis has been re-assigned to the genus Campylobacter, and B. melaninogenicus has been reclassified and divided into Prevotella melaninogenica and P. intermedia) (Table 3) [12]. Additional genera harboring re-assigned former Bacteroides group pathogens include Dialister, Megamonas, Mitsuokella, Tannerella, Tissierella, and Alistipes. The biology and ecology of Bacteroides spp., both as commensal symbionts and virulent pathogens, is summarized elsewhere [12].

Table 3.

Species of the Genus Bacteroides

Species	Proportions reported from clinical isolates^*	Site with highest proportion
B. acidifaciens
B. buccae
B. caccae	2.8%–3.5%	Appendix
B. capillosus	0.4%–8.3%	Bone
B. caprocola
B. coprosuis
B. eggerthii
B. finegoldia
B. fragilis	11.1%–61.2%	Blood
B. helicogenis
B. intestinalis
B. massilinensis
B. nordii
B. oris
B. ovatus	3.0%–12.5%	Bone
B. plebeius
B. putredinis	0.4%–0.6%	Appendix
B. pyogenes
B. salyersai
B. stercoris	1.8%–2.0%	Appendix
B. suis
B. tetris
B. thetaiotaomicron	7.6%–23.3%	Lower extremity soft tissue
B. uniformis	2.3%–6.9%	Bone
B. ureolyticus
B. vulgatus	4.8%–22.3%	Foot

Species not enumerated may be considered “atypical” pathogens. From Murphy and Frick [12].

Anaerobic infections are usually polymicrobial [17], although B. fragilis is the only bacterium identified to date that can cause abscess formation as the sole infecting organism. Of relevance to wounds, necrotizing soft tissue infections are usually polymicrobial, with Bacteroides spp. representing about 7% of anaerobic isolates in one study [18]. In general, the organisms identified in soft tissue infections reflect the normal flora found adjacent. Human bite wounds (including clenched-fist injuries) reflect oral flora (e.g., Prevotella spp., Fusobacterium spp., and Peptostreptococcus spp., but usually not Bacteroides spp., although the latter have been identified as pathogens with dog- and cat-bite injuries [19].

Vibrio is a genus of facultative anaerobic gram-negative bacilli possessing a curved-rod shape (comma shape), several species of which can cause disease in human beings. Typically found in sub-tropical salt water [20], most disease-causing species are associated with gastroenteritis (usually associated with eating undercooked seafood), but can also infect open wounds and cause sepsis, which can be fatal. Among more than 75 known species of Vibrio, pathogenic Vibrio spp. include V. cholerae (the causative agent of cholera), V. alginolyticus [21], V. parahaemolyticus, and V. vulnificus (a cause of necrotizing soft tissue infection). Vibrio cholerae is generally transmitted by contaminated water. Patients with non-cholera Vibrio wound infection or sepsis are often critically ill and may deteriorate rapidly. Optimal therapy consists of prompt initiation of effective antibiotic therapy (doxycycline or a fluoroquinolone); aggressive fluid resuscitation and vasopressors if needed; and expeditious surgical evaluation and early debridement of the infected wound.

Aeromonas is a genus of gram-negative, facultative anaerobic, rod-shaped bacteria [22] that resemble members of the family Enterobacteriaceae morphologically. The most important pathogen is A. hydrophila, but most of the 28 described species have been associated with human diseases. The organisms are ubiquitous in soil and fresh and brackish water. Aeromonas spp. cause opportunistic systemic disease in immunocompromised patients, diarrheal disease in otherwise healthy individuals, and wound and other soft-tissue infections [23].

The two major diseases associated with Aeromonas spp. are gastroenteritis and wound infections, with or without bacteremia. Gastroenteritis typically occurs after the ingestion of contaminated water or food, whereas wound infections result from exposure to contaminated water or soil. In its most severe manifestation, Aeromonas spp. can cause necrotizing soft tissue infections. Although some potential virulence factors (e.g., endotoxins, hemolysins, enterotoxins, adherence factors) have been identified, their precise roles are unknown. In a comparative study [24], Vibrio spp. appeared to be more virulent compared with Aeromonas spp., causing more acute respiratory failure and the need for intensive care, but there was no difference in death rates.

Anaerobic gram-positive bacilli

The family Actinomycetaceae contains three potentially pathogenic genera: Actinomyces, Nocardia, and Streptomyces. Actinomyces is a genus of pleomorphic, gram-positive, facultative anaerobic bacteria, of which there are more than 35 species [25]. Actinomyces meyeri and A. israelii are both obligate anaerobes, but all grow best under anaerobic conditions. Actinomyces spp. may form endospores, and, whereas individual bacteria are rod-shaped, Actinomyces colonies form branched networks of hyphae reminiscent of fungus. The taxonomic designation thus suggests that they are fungi, but they are not, having been misclassified based on morphology at the time of their discovery. Actinomyces spp. are ubiquitous in soil and in the commensal microbiota (skin, oral cavity, gut, and vagina) of human beings and livestock. They are also potential pathogens of their hosts, usually when invasive through wounds. As with other opportunistic infections, persons with immunodeficiency are at higher risk. In all of the preceding traits and in their branching filament formation, they bear similarities to Nocardia spp. In common with other anaerobes, Actinomyces spp. are fastidious and thus challenging to culture and isolate; thus, a negative result of microbiology analysis does not rule out infection.

Many Actinomyces spp. are opportunistic pathogens of human beings and other mammals, particularly in the oral cavity, chest, or abdomen/pelvis [26]. In rare cases, these bacteria can cause actinomycosis, which is characterized by abscess formation in the mouth, lungs, or gastrointestinal tract, and caused most frequently by A. israelii. Actinomycosis may be considered when a patient has chronic progression of disease across natural tissue planes with mass effect, sinus tract development that may heal and recur, or refractory infection after a typical course of antibiotic agents.

Aerobic gram-positive bacilli

Corynebacterium is a diverse genus of pleomorphic aerobic gram-positive bacilli. In some phases of life, they are club-shaped, which inspired the taxonomy (coryneform means “club-shaped”). They are widely distributed in nature in the microbiota of animals and human beings, and are mostly innocuous, although they can occasionally capitalize opportunistically by access via wounds or impaired host defenses. Non-pathogenic corynebacteria are referred to collectively as diphtheroids. The most notable human pathogen is C. diphtheriae, which, in addition to causing diphtheria, an acute, contagious infection characterized by pseudomembranes of dead epithelial cells, leukocytes, erythrocytes, and fibrin that form around the tonsils and back of the throat, can occasionally infect wounds [27], the vulva, the conjunctiva, and the middle ear. Other human pathogens of the species include C. amycolatum, C. striatum, C. jeikeium, C. urealyticum, and C. xerosis.

The genus Arcanobacterium are gram-positive, non-motile, facultatively anaerobic bacilli. There has been a great deal of taxonomic re-assignment among the genera Corynebacterium, Actinomyces, Arcanobacterium, and Trueperella. Arcanobacterium spp. are distributed widely in nature in the microbiota of animals and human beings and are mostly innocuous. Some can cause disease in humans (e.g., A. haemolyticum, formerly C. haemolyticum). As with their cousins in the genera Corynebacterium and Trueperella, they usually are not pathogenic but can occasionally opportunistically capitalize on atypical access to tissues (via wounds) or weakened host defenses. An A. haemolyticum infection is any of several types of infection with the gram-positive bacillus, including acute pharyngitis, and it may cause an exanthem characterized by an erythematous, morbilliform, or scarlatiniform eruption involving the trunk and extremities. Arcanobacterium haemolyticum has been isolated from diabetic foot infections [28].

Non-tuberculous mycobacteria

Mycobacteriaceae are a family of small, rod-shaped bacilli that can be classified into three main groups for the purpose of diagnosis and treatment: Mycobacterium tuberculosis complex, which can cause tuberculosis – M. tuberculosis, M. bovis, M. africanum, M. microti, and M. canetti; M. leprae and M. lepromatosis, which cause leprosy (Hansen disease); non-tuberculous mycobacteria (NTM), also known as environmental mycobacteria, atypical mycobacteria, and mycobacteria other than tuberculosis (MOTT), which are mycobacteria that do not cause tuberculosis or leprosy, and represent all other mycobacteria that cause disease. The number of identified and cataloged NTM species has been increasing rapidly, now numbering more than 125. The increase is atributable to improved isolation and identification techniques. Non-tuberculous mycobacteria can cause pulmonary infection resembling tuberculosis, lymphadenitis, skin disease, or disseminated disease. In 1959, botanist Ernest Runyon put these human disease-associated bacteria into four groups (Runyon classification) (Table 4) [29]. Many Mycobacterium spp. remain unclassified.

Table 4.

Runyon Classification of Mycobacteria

• Photochromogens (Type I)

• Develop pigments in or after being exposed to light

• Mycobacterium kansasii, M. simiae, M. marinum

• Scotochromogens (Type II)

• Become pigmented in darkness

• M. scrofulaceum, M. szulgai

• Non-chromogens (Type III)

• Prevalent opportunistic pathogens

• M. avium complex (MAC), M. ulcerans, M. xenopi, M. malmoense, M. terrae, M. haemophilum, M. genavense

• Rapid growers (Type IV)

• Four well-recognized, pathogenic, rapidly growing non-chromogenic species^*

• M. chelonae, M. abscessus, M. fortuitum, M. peregrinum

• Other examples cause disease rarely

• M. smegmatis, M. flavescens

Mycobacterial species listed are exemplary, and not a comprehensive listing except for the four^* pathogenic non-chromogenic species that cause soft tissue infections. Many Mycobacterium spp. remain unclassified.

Human disease is believed to be acquired from environmental exposure; there are no reports of animal-to-human or human-to-human transmission of NTM. Most soft tissue infections are caused by the “rapid-growers” (Runyon Type IV) [30] and are introduced by injection or direct traumatic inoculation. Mycobacteria are ubiquitous in nature and can be found in soil, dust, rocks, bio-aerosols, and water [31 –35]. These organisms have been increasingly identified from austere environments (i.e., low nutrients, low pH, and temperature extremes). Biofilm formation is a successful survival strategy for these hydrophobic organisms.

Mayo Clinic researchers found that the incidence of cutaneous NTM infection increased three-fold between 1980 and 2009 in a population-based study of residents of Olmsted County, Minnesota [36]. The most common species were M. marinum (45% of cases); and M. chelonae and M. abscessus, together accounting for 32% of patients. Mycobacterium chelonae infection outbreaks, as a consequence of tattooing with infected ink [37], have been reported in the United Kingdom and the United States.

Rapidly growing NTMs are implicated in catheter infections, ophthalmic surgical procedures, skin and soft tissue infections (especially SSIs after cosmetic or cardiac operations), and pulmonary infections [38 –49].

Mycoplasma

The family Mycoplasmataceae consists of two related genera, Mycoplasma spp. and Ureaplasma spp., bacteria that lack a cell wall around their cell membrane. Thus, also being pleomorphic in appearance, they cannot be characterized by gram staining, or by whether they are cocci or bacilli. Without a cell wall, they are unaffected by many common antibiotic agents such as penicillins or other beta-lactam antibiotic agents that target cell wall synthesis. Mycoplasma species are the smallest bacterial cells yet discovered and can survive without oxygen, They can be parasitic or saprotrophic. More than 125 Mycoplasma spp. have been described, a dozen or more of which are pathogenic in human beings, including M. pneumoniae, which is an important cause of atypical pneumonia and other respiratory disorders.

Only isolated case reports of Mycoplasma SSIs have been reported [50,51], mostly caused by M. hominis. Such infections have been reported after cardiac surgical procedures; heart, kidney, and lung transplantation; knee arthroplasty; neurosurgical procedures including spine operations and ventriculoperitoneal shunt infection; obstetric and gynecologic operations; and prostatectomy, among others.

Among the eight identified Ureaplasma spp., U. parvum is recognized as commensal flora of the female genital tract, whereas U. urealiticum is recognized for its ability to cause invasive infection [52 –55]. Reports of invasive U. urealiticum are few; invasive infection has been reported after cardiac surgical procedures, solid-organ transplantation, and hysterectomy [52 –55]. Some of the reports describe co-infection with M. hominis [56 –60].

Footnotes

Author Disclosure Statement

No competing financial interests exist.

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