Musculoskeletal and Soft Tissue Aeromonas Infection: An Environmental Disease

Musculoskeletal and Soft Tissue Aeromonas Infection: An Environmental Disease

LESLEY M. VOSS, M.B.,Ch.B.,* K. HABLE RHODES, M.D., Section of General Pediatrics and Pediatric Infectious Diseases; KENNETH A. JOHNSON, M.D.,t Section ofOrthopedic Surgery

During a 4-year period from November 1985 to November 1989, Aeromonas was isolated from wounds and soft tissues with clinical evidence of infection in 28 patients at our institution. Of the 28 patients, 23 (82%) had sustained an acute open or penetrating injury, more than half of which (13 of the 23) were water-related trauma. One patient had Aeromonas osteomyelitis. Five patients had no history of trauma, and three of these five had an underlying chronic disease. Treatment included debridement and antimicrobial agents. Susceptibility testing on 25 isolates from 23 patients showed uniform resistance to ampicillin and considerable resistance to cefazolin sodium (68%), but all isolates were sensitive to gentamicin sulfate, cefuroxime sodium, and the third-generation cephalosporins. Aeromonas has increasingly been recognized as a cause of soft tissue and musculoskeletal infections, usually after traumatic injury in immunocompetent hosts and occasionally de novo in compromised hosts. This organism causes various infections, including cellulitis, gas gangrene, myonecrosis, fulminant necrotizing infections, and osteomyelitis.!" Initially, most severe cases were reported in immunosuppressed hosts," but fatalities have also occurred after trauma in normal hosts." This gram-negative bacillus, which is found in natural water sources, can contaminate aquatic wounds and produce erythema, edema, and purulent drainage," In addition, however, Aeromonas is associated with nonaquatic injuries, and nosocomial wound infections have also been substantiated. The recent use of medicinal leeches in microvascular operations has led to several soft tissue infections with Aeromonas, which apparently is present in the gut flora of leeches.t'? Awareness of this organism as a pathogen is necessary so that adequate treatment regimens, including aggressive debridement and appropriate antibiotic agents,

*Current address: Auckland Hospital, Auckland, New Zealand. tMayo Clinic Scottsdale, Scottsdale, Arizona. Address reprint requests to Dr. K. H. Rhodes, Section of General Pediatrics and Pediatric Infectious Diseases, Mayo Clinic, Rochester, MN 55905. Mayo Clin Proc 67:422-427, 1992

can be initiated to prevent a fulminant and occasionally fatal infection. In this report, we review the clinical and microbiologic data of isolates of Aeromonas from wound and soft tissue cultures for a 4-year period at our institution. We also describe the results of antimicrobial susceptibility testing against commonly used drugs.

METHODS We reviewed data from Aeromonas isolates of infected wound and soft tissue sites in patients examined at our institution or its affiliated hospitals during the 4-year period from November 1985 to November 1989. The medical records of the patients were reviewed for initial symptoms and signs, exposure to water or other environmental factors, mode of acquisition, predisposing conditions, management, and outcome. Clinical evidence of infection included exudates and other localized signs of spreading infection such as progressive erythema, tenderness, and swelling. Positive cultures were included if the specimens had been appropriately collected from exudative wounds or from tissues or exudates deep within the wound at the time of surgical debridement when infection was evident clinically. Before aspiration of exudates, antiseptics (iodophors or povidone-iodine) were applied to the skin. The aspiration specimens and those obtained during surgical procedures were put in appropriate 422

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vials and sent immediately to the laboratory in accordance with the collection and transport procedures used at our institution. 11 All swabs from wounds or soft tissue were plated onto blood, eosin-methylene blue, and colistin-nalidixic acid agar and into thioglycollate broth. All oxidase-positive gramnegative bacilli were identified with conventional biochemical media. Further appropriate biochemical tests were done as necessary.P Antimicrobial susceptibility testing was performed by an agar-dilution method." CLINICAL AND MICROBIOLOGIC DATA During the 4-year period of study, 42 isolates of Aeromonas were cultured from wound and soft tissue sources in 28 patients, most (90%) of whom were male. The mean age of the patients was 32 years (range, 8 to 85 years). Only three patients had a predisposing condition: chronic vascular insufficiency in two patients (one of whom also had diabetes mellitus) and chronic lymphocytic leukemia in one patient. Sixty percent of specimens for culture were from a lower limb, 30% from an upper limb, and 10% from the head or neck. Almost 70% of the isolates were obtained during summer, and 43% of the total were directly related to water injuries. Aeromonas alone was isolated in 10 patients, 7 of whom had a water-related injury (Table 1). These infections were treated with appropriate antibiotics with or without debridement, although in two patients, susceptibility tests were not performed and antibiotics were administered empirically. All patients had uncomplicated resolution of the infection after appropriate therapy was instituted. One patient had Aeromonas osteomyelitis. In approximately two-thirds of the patients, Aeromonas was cultured together with up to seven other gram-positive or gram-negative bacterial organisms, a finding consistent with environmental contamination. In those patients with mixed cultures, assessing the contribution of Aeromonas to the infective process was difficult. Of those patients with postoperative or chronic infection and polymicrobial cultures, half responded to parenterally or orally administered antibiotics only; the rest also required debridement. In those patients with acute infection and mixed cultures, debridement used in combination with antibiotics produced resolution of the infection. Of the 28 study patients, 23 (82%) had an acute open or penetrating injury. In 13 of these 23 patients, the initial injury had occurred in lake or river water; the rest of the patients had a nonaquatic injury. Five patients, however, had no history of an injury. Three of these patients had an abscess or cellulitis, and two had infected chronic ulcers. The two patients with chronic ulcers had underlying chronic vascular insufficiency, and one also

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had diabetes mellitus. One patient with only an abscess had chronic lymphocytic leukemia. REPORT OF ILLUSTRATIVE CASES Four cases of Aeromonas infection are described in detail to exemplify the characteristic features. Cases 1, 2, and 3 demonstrate water-related injuries and resultant infections. Although two of these patients (cases 1 and 2) had pure Aeromonas infections, one (case 3) had a polymicrobial infection, which frequently occurs after trauma with contamination from environmental sources. The fourth case report describes the spontaneous onset of acute Aeromonas infection in a patient who had no history of trauma but had an underlying chronic disease. Case I.-A 33-year-old man sustained a puncture wound on the lower part of his right leg while floating in an inner tube on a river. The wound was initially cleaned and sutured, but 3 days later, it became erythematous, swollen, and tender. The patient underwent debridement, at which time periosteal involvement of the tibia was noted and antibiotics were administered parenterally. Aeromonas resistant to ampicillin and cefazolin sodium was isolated from wound specimens obtained at operation. The wound healed, and no further complications occurred. Case 2.-A 41-year-old man sought medical assistance because of chills, fever, and an erythematous area (5 by 8 em) of soft tissue swelling above the left medial malleolus. The swelling first became clinically apparent 9 months after he had sustained a compound fracture of his ankle, which occurred in a lake at the time of an airplane accident. Roentgenograms showed destructive changes in the articulating surface of the distal left tibia and along the dome of the talus, consistent with osteomyelitis (Fig. 1). Tomograms of the distal left tibia showed serpentine tracts of osteomyelitis that extended from the joint space proximally for about 7 cm. A large bony defect of the distal tibia that consisted of central sclerosis and a sequestrum and a second bony defect of the distal tibia posteriorly were visible on the tomograms (Fig. 2). At the time of surgical debridement, purulent material was noted. Histopathologically, osteomyelitis that involved the distal anterolateral tibia was evident. Only Aeromonas grew from cultures of bone and soft tissue. Treatment consisted of wide surgical debridement, a parenterally administered antibiotic, and open packing of the wound. Ankle stability was provided by application of an external fixator and transfixion pins through the talus and tibia. After 24 days with twice-daily whirlpool treatments and packing, the wound was clean, and granulation tissue was satisfactory. A Papineau-type cancellous bone graft from the iliac crest was then inserted into the ankle region. Three months later, the ankle was thought to be fused, and the external fixator was removed.

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Table I.-Clinical Details of 10 Study Patients With Pure Cultures of Aeromonas Age (yr) and sex

Site affected

Initial manifestation

Exposure to water

Predisposing conditions

26M

Leg

Infected laceration

Yes

No

42M

Leg

Infected laceration

Yes

No

22M

Foot

Infected puncture wound

Yes

No

33 M

Leg

Infected puncture wound

Yes

No

15M IBM 41M 9M

Head Neck Leg Foot

Infected laceration Wound infection Osteomyelitis Cellulitis

Yes Yes Yes No

No No No No

17M

Scalp

Infected laceration

No

No

74M

Hand

Abscess

No

CLL*

Antibiotics used

Debridement

Outcome

Penicillin Ampicillin, clavulanic acid Ampicillin, c1avulanic acid Cefadroxil monohydrate Cefazolin sodium Penicillin Gentamicin sulfate Cefotaxime sodium Nafcillin sodium Gentamicin Cefazolin Cefadroxil Cefadroxil Cefoperazone dihydrate Mezlocillin sodium Gentamicin Cefazolin Cefadroxil Cefadroxil Tetracycline hydrochloride Ciprofloxacin hydrochloride

No

Resolved

No

Resolved

No

Resolved

Yes

Resolved

No No Yes Yes

Resolved Resolved Resolved Resolved

No

Resolved

Yes

Resolved

*CLL = chronic lymphocytic leukemia.

Case 3.-In an 8-year-old boy, a septic olecranon bursitis developed after he fell from a bridge into a dirty creek. An abrasion of the left elbow became erythematous and tender within 24 hours. Aeromonas was isolated in culture specimens obtained at debridement, along with Klebsiella oxytoca, Enterobacter aerogenes, Clostridium perfringens, Escherichia coli, and group D streptococcus. At operation, a small puncture wound was found, which healed with use of a broad-spectrum parenterally administered antibiotic agent. Case 4.-In a 74-year-old man with a history of chronic lymphocytic leukemia, autoimmune hemolytic anemia, and coronary artery disease, a tender swelling developed in the right middle finger. The patient had no history of trauma. An abscess and cellulitis were diagnosed, and the abscess was drained. Culture specimens obtained at the time of drainage grew Aeromonas sensitive to cefazolin, gentamicin sulfate, and ciprofloxacin hydrochloride. After treatment with ciprofloxacin for 14 days, the infection resolved, and no further problems ensued. RESULTS OF SUSCEPTIBILITY TESTING Susceptibility testing was performed on 25 isolates of Aeromonas from 23 patients (Table 2). As expected, all were resistant to ampicillin, with a 90% minimal inhibitory con-

centration of more than 16 ug/ml; 68% were resistant to cefazolin, with a 90% minimal inhibitory concentration of more than 16 ug/ml. Resistance to mezlocillin sodium, cefoxitin sodium, and tetracycline hydrochloride was noted in one isolate each. All isolates were sensitive to amikacin sulfate, gentamicin, cefuroxime sodium, and third-generation cephalosporins (cefoperazone dihydrate, ceftizoxime sodium, and ceftazidime). The initial empiric choice of antimicrobial agents included penicillins, penicillinase-resistant penicillins, firstand third-generation cephalosporins, aminoglycosides, clindamycin, imipenem, ciprofloxacin, and trimethoprimsulfamethoxazole. Among the study patients, 62% received more than one antibiotic during the course of treatment. DISCUSSION During the past 2 decades, Aeromonas species have increasingly been implicated as a cause of disease in humans. This gram-negative, oxidase-positive bacillus has been associated with several conditions, particularly gastroenteritis, skin and soft tissue infections, infections of the respiratory tract, meningitis, endocarditis, osteomyelitis, and septicemiaf":" the skin and soft tissues are the most common sites of extraintestinal infection. Although the organism was initially reported as a pathogen in immunosuppressed patients,"

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Fig. I (case 2). Preoperative roentgenogram, showing destructive changes abouttibiotalar joint, consistent withosteomyelitis, in 41year-old manwhohad sustained a compound fracture of left ankle. Aeromonas is now known to cause severe disease in immunocompetent hosts as well. Aeromonas has been isolated predominantly from aquatic environments but also from various other sources, including food and soil. 18 It has been implicated as a cause of infection after traumatic water-related injuries, including automobile, motorcycle, boating, and swimming accidents and even a piranha bite. 1•3,4,6, 19,20 In our series, injuries in an aquatic environment were the most common type-43% of infections were associated with a water-related (lake or river) injury. This observation is in contrast to the findings of a recent review of Aeromonas wound infections in which only I of 27 cases had resulted from water-related trauma." The seasonal distribution of cultures is probably explained by increased exposure to water, especially from water sports, in the summer. Aeromonas has infrequently been reported as a cause of osteomyelitis. 3, 19,22. 24 Of the six cases that have been reported, four occurred in healthy hosts after water-related injuries, one occurred in a soil-contaminated fracture wound, and one occurred in an open fracture wound either environmentally contaminated at the time of traumatic injury or nosocomially contaminated during hospitalization for numerous surgical procedures. Our patient with osteomyelitis sought medical attention many months after sustaining a traumatic injury, which initially was environmentally contaminated. Thus, Aeromonas should be considered in any water-contaminated or environmentally contaminated wound or open fracture with gram-negative bacilli. Aeromonas septic arthritis, with isolation of the organism from

Fig. 2 (case 2). Anteroposterior tomogram of same patient as depicted in Figure I, showing serpentine tractsof bone dissolution in distaltibia andformation of sequestrum. synovial fluid and blood, has been reported in three patients with leukemia who had no traumatic wounds.v-" A possible portal of entry into the general circulation of patients with leukemia may be areas of breakdown in the intestinal barriers attributable to chemotherapeutic agents or to infiltration by leukemic cells. Aeromonas may be nosocomially acquired. The organism has been found in hospital water supplies" and is known to survive on bench tops and on moistened paper towels." In a review by Washington," 30% of the patients had acquired Aeromonas after admission to the hospital. He was unable to identify the environmental origin, and surveillance cultures of water sources and equipment for inhalational therapy were negative. Periodic culture surveillance procedures for environmental contaminants in our hospitals have not demonstrated Aeromonas, and we found no evidence to establish nosocomial acquisition in any of our patients. Initially, three of our patients were examined elsewhere, and initial culture results were unavailable. In addition, some

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Table 2.-ln Vitro Susceptibilities of 25 Strains of Aeromonas Species Minimalinhibitory concentration(Ilglml) Drug Amikacinbase Ampicillin Cefazolin.sodium

Cefoperazone dihydrate Cefoxitin sodium Ceftazidime Ceftizoxime sodium Cefuroxime sodium Gentamicin sulfate Mezlocillinsodium Tetracycline hydrochloride

50%

Range

inhibition

8 >16 ~8 to >16

>16 >16

~16

~8

to >16 ~8

<8 ~8

1 ~16 to >64

8

16 8 8 8

8

1 16

90%

inhibition 8 >16 >16 16 8

8 8 8

1

16

1 to >8

cultures may have been negative because of limited sampling at the time of initial assessment or debridement. Aeromonas has been considered a contaminant because it is often just one of many gram-negative bacilli and grampositive cocci isolated from a wound. In our review, 64% of cultures had multiple organisms, and the contribution of Aeromonas to the infective process was difficult to establish. When only Aeromonas is isolated from infected wounds, however, a pathogenic role is implicated. Aeromonas should be regarded as an important contributing pathogen, particularly when the culture specimen is obtained under sterile conditions at the time of debridement. Antimicrobial susceptibility testing confirmed uniform resistance to ampicillin, which has been established as being due to production of p-Iactamase. 3o This mechanism, however, is not the complete answer because the addition of clavulanic acid, an enzyme inhibitor, does not result in susceptibility of the isolate.t''-" We found considerable resistance to cefazolin, as has been noted by other investigators;32,33 this observation suggests that first-generation cephalosporins have a limited role in treating Aeromonas infections. Recent reports also indicate that resistance is increasing in Aeromonas isolates, both patient-acquired and environmentally acquired.":" This chloramphenicol-streptomycin-tetracycline resistance seems to be plasmid mediated; however, the aminoglycosides except streptomycin, the third-generation cephalosporins, and the oxyquinolones provide adequate coverage against Aeromonas isolates.v" Because of the results of our susceptibility testing, we recommend aminoglycosides, mezlocillin, and third- or some second-generation cephalosporins or tetracyclines (in patients older than 9 years of age in whom oral therapy can be used) as initial treatment of Aeromonas infection until spe-

cific results of susceptibility testing are available. Whether parenteral or oral therapy is necessary depends on several factors, including the site of infection and the need for high serum levels of the drug for optimal penetration of tissues, as in the treatment of osteomyelitis or infections in immunocompromised hosts. CONCLUSION Although Aeromonas wound infections usually remain localized and complete recovery usually ensues after appropriate therapy in immunocompetent hosts (as seen in our study), overwhelming infections have been substantiated in healthy and in immunocompromised hosts. Cases of severe cellulitis," ecthyma gangrenosum," and necrotizing myositis1,2,39,40 have been reported. Such infections have resulted in amputations and occasionally death despite early and appropriate therapy.'> Because of the potential invasive nature of Aeromonas, this organism should be suspected in all water-related trauma. Management of Aeromonas wound and soft tissue infections should be individualized but should include early aggressive debridement and appropriate orally or parenterally administered antibiotics. REFERENCES 1. Deepe GS Jr, Coonrod JD: Fulminant wound infection with Aeromonas hydrophila. South Med J 73:1546-1547,1980 2. Geller HS, Tofte RW, Cunningham BL: Aeromonas hydrophila wound infection of the hand initially presenting as clostridial myonecrosis. J Hand Surg 8:333-335, 1983 3. Karam GH, Ackley AM, DismukesWE: PosttraumaticAeroArch Intern Med monas hydrophila osteomyelitis. 4.

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