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Outbreak of Aeromonas hydrophila WoundInfections Associated with Mud Football Hassan Vally,1,2 Amanda Whittle,3 Scott Cameron,2 Gary K. Dowse,1 and Tony Watson1
1Communicable Disease Control Branch, Department of Health, Perth, 2National Centre for Epidemiology and Population Health,Australian National University, Canberra, and 3South West Population Health Unit, Department of Health, Bunbury, Australia On 16 February 2002, a total of 26 people presented to the emergency department of the local hospital in the
rural town of Collie in southwest Western Australia with many infected scratches and pustules distributed
over their bodies. All of the patients had participated in a “mud football” competition the previous day, in
which there had been ∼100 participants. One patient required removal of an infected thumbnail, and another
required surgical debridement of an infected toe. Aeromonas hydrophila was isolated from all 3 patients from
whom swab specimens were obtained. To prepare the mud football fields, a paddock was irrigated with water
that was pumped from an adjacent river during the 1-month period before the competition. A. hydrophila
was subsequently isolated from a water sample obtained from the river. This is the first published report of
an outbreak of A. hydrophila wound infections associated with exposure to mud.
Members of the genus Aeromonas are facultative an- by exposure to contaminated water or soil [4–8]. These aerobic, nonsporulating gram-negative bacilli that are infections occur sporadically and infrequently, and they ubiquitous inhabitants of fresh and brackish water [1].
are more common in warmer climates [5, 7]. Wound Aeromonas species have been found in a variety of infections caused by A. hydrophila often progress rap- aquatic environments, including lakes, rivers, streams, idly and may require surgical debridement or the am- springs, rainwater, swimming pools, and seawater, and putation of limbs or digits [6]. Fatal Aeromonas wound have also been isolated from tap water and soil [2–4].
infections in healthy adults have also been reported [9, These species have been recognized as pathogens of 10]. Treatment of Aeromonas wound infections is com- fish, reptiles, and amphibians for many decades, but it plicated by the fact that members of this genus are is only recently that they have been recognized as sig- universally resistant to penicillin (the result of the pres- nificant human pathogens [1]. In humans, infections ence of chromosomal b-lactamase), rendering standard caused by Aeromonas species generally result in either empirical antibiotic treatment for common streptococ- acute or chronic gastrointestinal illness, septicemia cal or staphylococcal wound infections ineffective [11].
in immunosuppressed individuals, or water- or soil- In this report, we describe an unusual outbreak of associated traumatic wound infections [4, 5].
wound infections caused by A. hydrophila in individuals Aeromonas wound infections are most commonly participating in a “mud football” competition in a small caused by Aeromonas hydrophila and have been re- rural town in the southwest of Western Australia. An ported after accidental puncture of the skin followed investigation was conducted to ensure that appropriateantibiotic therapy was administered to patients, to iden-tify factors contributing to the outbreak, and to add toour knowledge of the clinical features of A. hydrophila Received 20 June 2003; accepted 3 December 2003; electronically published Financial support: Western Australia Department of Health and Commonwealth Department of Health and Aging (jointly funded scholarship to H.V.).
Reprints or correspondence: Dr. Gary Dowse, Communicable Disease Control PATIENTS AND METHODS
Branch, Dept. of Health, Western Australia, PO Box 8172, Perth Business Centre,Perth WA 6849, Australia ([email protected]).
Background.
Clinical Infectious Diseases
2004; 38:1084–9
residents situated 200 km south of Perth, the capital of 2004 by the Infectious Diseases Society of America. All rights reserved.
Western Australia. On Sunday, 17 February 2002, a total 1084 • CID 2004:38 (15 April) • Vally et al.
of 26 persons who had participated in a charity mud footballcompetition in Collie on the previous day presented to theemergency department at Collie Hospital with infectedscratches and pustules over their torsos and limbs. Most personsreported 20–30 lesions, with some reporting 1100 lesions. Onepatient required removal of an infected thumbnail at the emer-gency department, and another required surgical debridementof an infected toe in the hospital the next day. Swab sampleswere obtained from lesions of 2 patients at the emergency de-partment, and A. hydrophila was identified from cultures ofthese swabs 2 days later. A third swab specimen obtained fromthe patient requiring surgical debridement also grew A. hydro-phila. Anecdotally, at least 16 mud football players, in additionto the 26 who presented at the emergency department, visitedtheir medical practitioners with similar symptoms, but no fur- Figure 1.
A game of mud football in Collie, Western Australia (15 ther data were obtained from these individuals.
February 2002; used by permission of Janine Kay, copyright 2002).
Eleven adult and 4 youth teams consisting of a total of ∼100 people were involved in the mud football competition. The games Antibiotic susceptibility testing of clinical isolates was com- were played between 1:30 pm and 4:00 pm in the afternoon on pleted using the NCCLS agar dilution method [12].
a midsummer day in which the maximum temperature reached To test water samples for Aeromonas species, 100 mL of water 26ЊC. Two football fields were used simultaneously for a round- was filtered through a 0.45-mm nitrocellulose membrane. This robin competition, with each game consisting of two 15-min membrane was then placed on a horse blood agar plate con- halves. A Rugby Union competition was played, which involved taining ampicillin (5 mg/L). After incubation overnight at 37ЊC, considerable physical contact, including players tackling and oxidase-positive colonies were further identified with the API wrestling each other for the ball in the mud (figure 1). Children 20E biochemical identification system.
who did not participate in the mud football competition wereprovided with their own mud pool.
Case series.
All 26 patients (or their parents) who pre- sented to the emergency department at Collie Hospital on Sun- Public health management of the infection outbreak.
day, 17 February, were interviewed. A questionnaire was used being notified of the outbreak of wound infections early on for the interview that addressed the clinical features and ex- Monday, 18 February, the Collie environmental health officer posure of the patients to mud and to river water. Other data compiled a list of mud football participants so that they could collected included the estimated number and location of skin be telephoned, assessed, and advised about the appropriate lesions, other presenting symptoms, preexisting medical con- management of their lesions. The next morning, putative Aero- ditions, and current systemic antibiotic treatment. Patients who monas species were reported by the Collie microbiology lab- had been prescribed systemic antibiotics before the identifi- oratory and sent to the Public Health Reference Laboratory in cation of A. hydrophila were advised to contact their medical Perth for speciation and antibiotic susceptibility testing. The practitioner to ensure that they were taking the recommended Communicable Disease Control Branch in Perth was notified antibiotics for treatment of Aeromonas infection. These patients by the Reference Laboratory of the cultures positive for Aero- were also followed-up to determine whether their antibiotic monas species and began to coordinate the response to this outbreak with the regional public health unit.
Environmental investigation.
The primary objective of the public health response was to football fields, the adjacent Collie River, and the irrigation ensure that all patients with Aeromonas infection were identified equipment was performed by the local environmental health and provided with appropriate treatment and that medical officer. In addition, a water sample was obtained from the river practitioners and the public were alerted to the possibility of near the inlet pipe for the irrigation pump and tested for tem- Aeromonas wound infections due to mud football or exposure perature, pH, and bacterial pathogens.
to river water. Letters and Aeromonas infection fact sheets were Laboratory methods.
faxed to local medical practitioners advising them to review plated onto horse blood agar plates. After overnight incubation their treatment of any mud football participants they had seen at 35ЊC, oxidase-positive colonies were further identified with with skin infections, particularly any antibiotic therapy that the API 20E biochemical identification system (BioMerieux).
was administered. The treatment recommended for suspected Aeromonas Infection and Mud Football • CID 2004:38 (15 April) • 1085
Aeromonas skin infections was oral ciprofloxacin, oral trimeth- alosporins (cefaclor and cephalexin), cephalothin, and colistin oprim-sulfamethoxazole, or intravenous ceftriaxone. Patients and were susceptible to norfloxacin, ciprofloxacin, gentamicin, who had presented to the emergency department on Sunday tobramycin, amikacin, trimethoprim, ceftriaxone, ceftazidime, were interviewed and were advised to contact their medical amoxicillin–clavulanate potassium, ticarcillin disodium–clavu- practitioner for reassessment of their antibiotic therapy. The lanate potassium, aztreonam, cefepime, and nitrofurantoin.
Communicable Disease Control Branch also released a local Case series.
Eighteen male and 8 female participants pre- media statement warning the public about the potential for sented to the emergency department on the Sunday after the serious infections after exposure to mud or untreated water mud football competition (table 1). The median age was 17 supplies and e-mailed all local microbiology laboratories to years (range, 3–43 years). Every patient was exposed to mud advise them to be alert for the presence of Aeromonas species during the mud football competition. In addition, all of the patients were directly exposed to river water after mud expo- Antibiotic susceptibility.
sure. Anecdotally, most patients were reported to have bathed clinical isolates of A. hydrophila were identical. These isolates in the river after playing in the mud; however, many patients were found to be resistant to amoxicillin, meropenem, oral ceph- also showered with river water before bathing in the river.
Characteristics of patients presenting to the emergency department with
Aeromonas skin infections associated with a game of “mud football.”
a Included у1 of the following: rash, malaise, myalgia, fever, rigors, headache, nausea, sore throat, b Infection resolved.
c Cultures of swab specimens were positive for Aeromonas hydrophila.
d Surgical debridement of toe required.
e Thumbnail was removed.
1086 • CID 2004:38 (15 April) • Vally et al.
The reported locations of lesions were the legs (77%), arms and the water temperature near the irrigation pipe was 23ЊC.
(58%), torso (35%), back (23%), chest (19%), buttocks (8%), The surface water temperature of the parts of the river that feet (8%), head (4%), and face (4%). The emergency depart- received more sun exposure was ∼30ЊC.
ment physicians who treated these patients reported that onlyscratches and abrasions were infected (i.e., there were no in-fected lesions on intact skin) and that up to 50% of all scratches DISCUSSION
were infected in some patients (M. J. Birch and B. Saharay, This report is the first description, to our knowledge, of an outbreak of cutaneous wound infections attributable to A. hy- Twenty-two players (85%) reported symptoms in addition drophila. Exposure to contaminated mud is likely to have been to infected lesions, including rash (69%), malaise (46%), fever the source of infection, although exposure of skin lesions to (35%), headache (35%), myalgia (31%), nausea (31%), rigors contaminated river water may also have played a role in this (8%), sore throat (4%), and earache (4%). Although rash was outbreak. Assuming all patients presenting to the emergency reported by a large number of patients, attending physicians department had A. hydrophila infections, as their clinical pre- did not substantiate this, suggesting that patients confused their sentation suggested, the attack rate for this outbreak was at numerous cuts and abrasions with the presence of a rash. None least 26%. Given that at least 16 other players with similar of the players who presented to the emergency department lesions were reported to have visited general practitioners, an reported any immunocompromising illnesses.
attack rate of 140% is possible. Patients reported up to 100 Antibiotic therapy was prescribed for 23 (88%) of the 26 infected lesions and pustules distributed over their body, and patients presenting to the Collie Hospital emergency depart- over one-half reported systemic symptoms, including fever, ment (table 1). In all of these patients, the empirically provided malaise, myalgia, headache, and nausea. Two patients also de- antibiotic therapy was unlikely to be effective against A. hy- veloped complications requiring surgical intervention.
drophila infection. After reassessment of their clinical status, 15 We could identify only 1 other report in the English language (65%) of the 23 patients had their antibiotic regimen changed.
literature of an outbreak of skin infections associated with ex- The treatment in 8 patients was not changed, because their skin posure to mud [13]. In this outbreak, college students were infections were resolving or had resolved. Of the 3 patients who reported to have developed perifolliculitis caused by Entero- were not initially prescribed antibiotics, 1 (patient 18) was pro- bacteriaceae after participation in a mud-wrestling social event.
vided ciprofloxacin after reassessment by her doctor. In addi- A subsequent case-control study indicated that trauma to the tion, the patient who required toe surgery (patient 15) was skin was a significant risk factor for infection after mud wres- administered intravenous ceftriaxone therapy after initially tling. Likewise, trauma to the skin is a well-documented risk being treated with flucloxicillin by emergency department factor for Aeromonas wound infections associated with expo- sure to water [6, 8]. In the current outbreak, multiple cuts and Environmental investigation.
abrasions, caused primarily by gravel and stubble in the football officer reported that the mud football fields were prepared by fields, are likely to have played an important role in facilitating plowing them to a depth of 500–600 mm and then irrigating Aeromonas wound infections. The presence of a large number them with water from the adjacent Collie River with sprinklers.
of lesions on the arms and legs, which would have been most At this time, the Collie River was low and had pooled as a frequently abraded during play, supports this hypothesis.
result of low rainfall levels (130% below average; Bureau of The method in which the mud was prepared for mud football Meteorology, Perth, Western Australia) during the previous 12 probably played an important role in this outbreak. The playing months. Water was pumped onto the fields with an irrigation field was irrigated with river water for a month before the pump and PVC pipes that formed part of an orchard irrigation competition, with watering increased a few days before the system 125 years old. The fields were irrigated each evening event to saturate the field. During this period, daytime tem- for 1 month before the mud football competition, with the peratures were warm, with maximum temperatures generally amount of watering increased a few days before the event to 125ЊC, and this may have provided an ideal environment for the growth of Aeromonas species in the soil. A previous study The fields were originally used to grow fruit trees, but these has shown that Aeromonas species can grow rapidly in soil when trees had been removed, and the fields had been fallow for 2 conditions are favorable (and when nutrients are available) years. The soil consisted of pea gravel and contained a stubble [14]. Survival curves in soil were characterized by a rapid in- that was a mixture of wild oats, wild turnips and radishes, field crease in cell numbers by several logs that lasted 1–2 weeks grasses, and weeds. A. hydrophila was cultured from the sample after initial contamination of the soil. Despite a decrease in the of river water obtained from near the irrigation pipe inlet at number of viable cells that occurred after this period of rapid the time of the outbreak. The pH of the river water was 7.5, growth, all of the strains studied were still present 140 days Aeromonas Infection and Mud Football • CID 2004:38 (15 April) • 1087
after initial contamination. Of importance, it was also shown would also be advisable to water the fields as close in time as that the virulence factors of Aeromonas species were preserved possible to the commencement of any event, so as to minimize after growth in soil [14]. Unfortunately, in the current inves- the opportunity for bacteria to multiply. And finally, it is rec- tigation, soil samples were not obtained at the time of the ommended that event organizers provide warm showers with outbreak to confirm the presence of Aeromonas species in the treated water and disinfectant for immediate antiseptic treat- In attributing causes for the current outbreak, it is worthwhile In conclusion, there are several public health lessons that to compare the inaugural mud football competition held in stem from this outbreak. First, organizers and local munici- March 2001 (in which there were no adverse effects reported) palities should be aware of, and consider the risks of, wound with the one conducted in February 2002. Although numbers infections associated with these types of events before giving of Aeromonas species in natural aquatic environments normally approval for them to proceed. Second, organizers should pro- increase in the summer [15], in the summer of 2001–2002, there vide participants with written advice alerting them to the risks, had been below-average rainfall, and the river level was very low and recommended management, of wound infections. It is also and had pooled, which may have further elevated the levels of important that doctors are educated to suspect Aeromonas spe- Aeromonas species in the river at the time of the 2002 compe- cies when there is potential contamination of a wound by water tition. In addition, in 2002, the football field was watered for a or soil. Finally, there is a need to develop safe mud-making whole month, but in 2001, the field was only watered for a few days before the event, providing less of an opportunity for Aero-monas organisms to multiply. Furthermore, an old irrigation Acknowledgments
pump and piping was used to water the field in 2002, whereaswatering in 2001 was completed manually with a free-standing We thank our colleagues at the South West Population Health pump and hose. Thus, the possibility that the irrigation system Unit, the Environmental Health Division of the Department may also have been a source of Aeromonas species in this outbreak of Health, and at the PathCentre Division of Microbiology and cannot be discounted, because this organism has been reported Infectious Diseases in Western Australia, for their help with to adhere to water distribution pipe surfaces [16].
this investigation; Ros Rabjones, Colin Wheadon, and Anne A major concern regarding Aeromonas infections is that they Foyer, for their assistance with the outbreak investigation; and may mimic streptococcal or staphylococcal soft-tissue infec- Professor Tom Riley, for reviewing the manuscript.
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