Tzu Chi Medical Journal
Volume 23, Issue 4 , Pages 119-122, December 2011

Polymicrobial bloodstream infection involving Aeromonas species: Analysis of 62 cases

  • Yu-Huai Ho

      Affiliations

    • Division of Infectious Diseases, Department of Medicine, Buddhist Tzu Chi General Hospital, Hualien, Taiwan
    • ,
  • Han-Chuan Chuang

      Affiliations

    • Division of Infectious Diseases, Department of Medicine, Buddhist Tzu Chi General Hospital, Taipei Branch, New Taipei City, Taiwan
    • ,
  • Chorng-Jang Lay

      Affiliations

    • Division of Infectious Diseases, Department of Medicine, Buddhist Tzu Chi General Hospital, Dalin Branch, Chiayi, Taiwan
    • School of Medicine, Tzu Chi University, Hualien, Taiwan
    • ,
  • Chun-Lung Wang

      Affiliations

    • Division of Infectious Diseases, Department of Medicine, Buddhist Tzu Chi General Hospital, Dalin Branch, Chiayi, Taiwan
    • School of Medicine, Tzu Chi University, Hualien, Taiwan
    • ,
  • Yeong-Shu Tsai

      Affiliations

    • Division of Infectious Diseases, Department of Medicine, Buddhist Tzu Chi General Hospital, Hualien, Taiwan
    • ,
  • Lih-Shinn Wang

      Affiliations

    • Division of Infectious Diseases, Department of Medicine, Buddhist Tzu Chi General Hospital, Hualien, Taiwan
    • School of Medicine, Tzu Chi University, Hualien, Taiwan
    • ,
  • Chen-Chi Tsai

      Affiliations

    • Division of Infectious Diseases, Department of Medicine, Buddhist Tzu Chi General Hospital, Dalin Branch, Chiayi, Taiwan
    • School of Medicine, Tzu Chi University, Hualien, Taiwan
    • Corresponding Author InformationCorresponding author. Division of Infectious Diseases, Department of Medicine, Buddhist Tzu Chi General Hospital, Dalin Branch, 2, Min-Sheng Road, Dalin, Chiayi, Taiwan. Tel.: +886 5 2648000; fax: +886 5 2648999.

Received 10 March 2011; received in revised form 13 June 2011; accepted 20 September 2011. published online 07 November 2011.

Article Outline

Abstract 

Objective

To better understand Aeromonas-involved polymicrobial bacteremia (AIPMB).

Materials and Methods

We conducted a retrospective analysis of patients with AIPMB admitted to three large referral hospitals in Taiwan between 2001 and 2008.

Results

Of a total of 62 patients with AIPMB, 22 had healthcare-associated infection and 40 had community-acquired infection. Enterobacteriaceae was the most common concurrent pathogen (82%). The leading underlying diseases/conditions in the affected patients were solid cancers (45%), recent gastric acid suppressant therapy (39%) and liver cirrhosis (26%). More than 95% of the Aeromonas isolates were susceptible to an aminoglycoside, a third- or fourth-generation cephalosporin, imipenem or ciprofloxacin. Antibiotic susceptibilities did not significantly differ between Aeromonas isolates in patients with healthcare-associated AIPMBs and those in patients with community-acquired AIPMBs. Coinfection with Enterobacteriaceae occurred more commonly in community-acquired AIPMB (93% vs. 64%; p=0.012).

Conclusions

AIPMB occurred commonly in patients with liver cirrhosis, solid cancers or recent gastric acid suppressant therapy. Enterobacteriaceae were the most common concurrent pathogens. Similar antibiotic profiles were found in Aeromonas isolates of healthcare-associated and community-acquired AIPMBs.

Key words: Aeromonas, Bacteremia, Polymicrobial

 

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1. Introduction 

The proportion of cases of bacteremia involving more than one species has ranged from 5% to 20% over the past 50 years [1]. Polymicrobial bacteremia is associated with malignancy, surgery and the placement of central venous catheters [1]. The mortality in patients with polymicrobial bacteremia is approximately twice that of patients with monomicrobial bacteremia [2], [3], [4].

Aeromonas, a member of the Aeromonadaceae family, is associated with a variety of human infections including gastroenteritis, wound infection and septicemia [5], [6], [7], [8]. Aeromonas infection is mainly acquired from the environment, especially contaminated water. In previous studies, there have been high proportions of polymicrobial infection where Aeromonas spp. have been involved in infections of the bloodstream [9], [10], [11], [12], [13], [14]. No study has yet delineated the clinical picture of Aeromonas-involved polymicrobial bacteremia (AIPMB), possibly because of a lack of sufficient cases in a single healthcare institution. We therefore conducted a retrospective multicenter study of AIPMB.

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2. Materials and methods 

This is a retrospective study of patients diagnosed with AIPMB admitted to Buddhist Tzu Chi General, Buddhist Dalin Tzu Chi General and Buddhist Taipei Tzu Chi General Hospitals in Taiwan between January 2001 and November 2008. Patient data, clinical and laboratory information were retrieved from the medical charts of the patients included in the study.

An AIPMB was defined as the simultaneous growth of an Aeromonas spp. and at least one other microbe from the blood culture of a patient with sepsis. Death was considered attributable to AIPMB if the patient died of unrelenting sepsis within 7 days after blood was sampled for culture where the culture was positive for Aeromonas species and one or more other microbes.

An AIPMB was considered healthcare-associated if the Aeromonas isolate was obtained from blood sampled ≥72 hours after admission to the hospital in a patient who had been asymptomatic upon admission, or in a patient who had received antineoplastic chemotherapy within the past 2 weeks, regardless of his or her symptoms at admission [15]. Acute respiratory failure was defined as the ratio of arterial oxygen tension (PaO2) to fractional inspired oxygen (FiO2) <200 [16]. The severity of the AIPMB was assessed using the Acute Physiology and Chronic Health Evaluation II (APACHE II) score less than 72 hours after the development of sepsis [17].

Gastric acid-suppressant therapy was defined as the use of a proton-pump inhibitor or a histamine H2 blocker for ≥7 days within 4 weeks before the emergence of an AIPMB.

2.1. Species identification and antimicrobial susceptibility 

Detection of bacterial growth from blood specimens was performed using the BACTEC 9240 blood culture system (BD Diagnostic Instrument Systems, Spark, MD, USA). Aeromonas species (Gram-negative bacilli) were identified by a positive oxidase test, growth on MacConkey agar, no growth on thiosulfate-citrate-bile-sucrose agar, and resistance to 150μg vibriostatic compound O/129 [5], [18]. Isolates were further confirmed with use of the Vitek II system (BioMérieux, Lyon, France), BD-Phoenix system (BD Diagnostic Instrument Systems, Spark, MD, USA) or API-20NE system (BioMérieux Marcy-I’Etoile, France). Additional tests, such as esculin hydrolysis, gas production from glucose, Voges-Proskauer reaction, ornithine decarboxylase and arginine dihydrolase production, were performed for the identification of bacterial species as necessary [5], [18].

In vitro antimicrobial susceptibilities of Aeromonas isolates were tested using the Kirby-Bauer disk-diffusion method or automated methods (Vitek II system or the BD-Phoenix system). All of the methods tested for gentamicin, amikacin, cefazolin, ceftriaxone, ciprofloxacin, piperacillin/tazobactam and imipenem. The BD-Phoenix system also ran tests including aztreonem. In the disk-diffusion method, antibiotics selected for testing also included cefmetazole, cefuroxime, ceftazidime, cefpirome and aztreonam. There were, however, some differences in the antibiotics selected for different Aeromonas isolates tested using the disk-diffusion method. The susceptibility breakpoints in the disk diffusion method were in accordance with those of the National Committee for Clinical Laboratory Standards for Enterobacteriaceae [19], while the susceptibility breakpoints in the automated methods were in accordance with those recommended by the Clinical and Laboratory Standards Institute M45-A [20].

2.2. Statistical analyses 

The Chi-square test or Fisher’s exact test was used to compare nominal data using the SPSS software package, version 11.0 (SPSS Inc, Chicago, IL, USA). A two-tailed p value of ≤0.05 was considered statistically significant.

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3. Results 

Of a total of 62 patients [mean age 62 years (range: 24–90 years); males: 33/62] with AIPMB, 22 had healthcare-associated infection and 40 had community-acquired infection. Four patients presented with necrotizing fasciitis, one with acute cholangitis and the others with primary bacteremia. Fifty-one patients (82%) had Enterobacteriaceae coinfection. Solid cancer (45%) was the most common underlying disease/condition, followed by gastric acid suppressant therapy (39%) and liver cirrhosis (26%). Forty-five patients (73%) presented with fever, 31 (50%) with thrombocytopenia and only 23 (37%) with leukocytosis. Eighteen (29%) patients had very severe disease (APACHE II score ≥20) and the overall mortality rate of AIPMB was 31% (19/62). The clinical characteristics of healthcare-associated and community-acquired AIPMBs are detailed in Table 1. The ratios of male gender and Enterobacteriaceae coinfection were significantly higher in community-acquired AIPMB than in healthcare-associated APIMB.

Table 1. Comparisons of clinical characteristics between healthcare-associated and community-acquired Aeromonas-involved polymicrobial bacteremias.
VariablePolymicrobial Aeromonas bacteremiap
Healthcare-associated N=22Community-acquired N=40
Age ≥65 y, n (%)7 (32)24 (60)0.063
Male, n (%)17 (77)16 (40)0.011
Enterobacteriaceae coinfectiona, n (%)14 (64)37 (93)0.012

Underlying disease/condition
ESRD, n (%)0 (0)2 (5)0.535
Recent intra-abdominal surgery, n (%)4 (18)8 (20)1.000
Solid cancer, n (%)13 (59)15 (38)0.171
Diabetes mellitus, n (%)5 (23)8 (20)1.000
Liver cirrhosis, n (%)6 (27)10 (25)1.000
Neutropenia, n (%)2 (9)1 (3)0.285
Gastric acid suppressant therapy, n (%)10 (45)14 (35)0.592

Laboratory and clinical features
Thrombocytopenia, n (%)11 (50)20 (50)1.000
Leukocytosis, n (%)8 (36)15 (38)1.000
Fever, n (%)17 (77)28 (70)0.751
Diarrhea, n (%)2 (9)1 (3)0.285
Shock, n (%)11 (50)16 (40)0.623
Abdominal pain, n (%)5 (23)12 (30)0.751
Acute renal failure, n (%)8 (36)7 (18)0.177
Acute respiratory failure, n (%)4 (18)7 (18)1.000
APACHE II score ≥20, n (%)7 (32)11 (28)0.947
Death due to sepsis, n (%)7 (32)12 (30)1.000

Abbreviations: APACHE=acute physiology and chronic health evaluation, ESRD=end-stage renal disease.

aSee Table 2 for details.

The concurrent pathogens for healthcare-associated and community-acquired AIPMBs are listed in Table 2. In community-acquired infection, Escherichia coli (23/40, 58%) was most commonly found, followed by Klebsiella spp. (9/40, 23%) and Enterobacter spp. (5/40, 13%). In healthcare-associated infection, Klebsiella spp. (5/22, 23%) were most frequently found, followed by Enterobacter spp. (5/22, 23%) and Acinetobacter spp. (5/22, 23%).

Table 2. Concurrent pathogens in patients with Aeromonas-involved polymicrobial bacteremias.
Concurrent pathogenHealthcare-associated infection (N=22), (%)Community-acquired infection (N=40), (%)
Escherichia coli3 (14)23 (58)
Klebsiella spp.6 (27)9 (23)
Enterobacter spp.5 (23)5 (13)
Proteus spp.1 (5)—
Serratia spp.—1 (3)
Morganella morganii—1 (3)
Citrobacter spp.1 (5)2 (5)
Pantoea agglomerans1 (5)—
Bacteroides spp.1 (5)1 (3)
Prevotella oralis1 (5)—
Coagulase-negative Staphylococcus1 (5)—
Streptococci spp.3 (14)3 (8)
Enterococcus spp.3 (14)2 (5)
Acinetobacter spp.5 (23)4 (10)
Stenotrophomonas maltophilia1 (5)—
Pseudomonas aeruginosa2 (9)—

The in vitro antimicrobial susceptibilities of Aeromonas isolates are listed in Table 3. There were 44 Aeromonas isolates tested by the disk-diffusion method, 12 by the Vitek II system and six by the BD-Phoenix system. The majority of Aeromonas isolates were susceptible to amikacin, gentamicin, ceftriaxone, ceftazidime, cefpirome, aztreonam, piperacillin/tazobactam, imipenem and ciprofloxacin. Thirty-nine out of 49 (80%) isolates tested were susceptible to cefuroxime, 15 of 62 (24%) were susceptible to cefazolin, and 23 of 41 (56%) were susceptible to cefmetazole. Antibiotic susceptibilities were not statistically different between community-acquired and healthcare-associated Aeromonas isolates.

Table 3. In vitro antibiotic susceptibilities of the Aeromonas isolates.
Antimicrobial agentsSusceptible isolatesp
Healthcare-associated infection n/N (%)Community-acquired infection n/N (%)
Gentamicin20/22 (91)35/40 (88)1.000
Amikacin21/21 (100)38/40 (95)0.541
Cefazolin7/22 (32)8/40 (20)0.298
Cefuroxime16/20 (80)23/29 (79)1.000
Cefmetazole8/15 (53)15/26 (58)0.956
Ceftriaxone20/22 (91)35/44 (88)1.000
Ceftazidime12/13 (92)18/19 (95)1.000
Cefpirome16/16 (100)26/26 (100)1.000
Aztreonam15/15 (100)23/24 (96)1.000
Piperacillin/tazobactam11/12 (92)27/28 (96)1.000
Imipenem21/22 (95)38/40 (95)1.000
Ciprofloxacin20/20 (100)35/37 (95)0.536

Abbreviation: n/N=Number of Aeromonas isolates susceptible to the antibiotic/number of Aeromonas isolates available for susceptibility testing.

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4. Discussion 

In agreement with previous reports [9], [10], [11], [12], [13], [14], the majority of AIPMBs were of primary bacteremia.

Aeromonas spp. exist in the environment, especially in fresh water. They are not considered as commensal organisms in the human gastrointestinal tract but can be isolated from feces in asymptomatic people [21]. Of all Aeromonas species, A hydrophila, A sobria and A caviae are the most common in human infection. In a mouse model, these three Aeromonas species were found to have higher colonization rates in colon tissue compared with other Aeromonas species [22]. Low-pH stomach acid has been reported to be effective in killing Aeromonas [23]. The high proportion of patients with AIPMB with prior gastric acid-suppressant therapy in this study therefore suggests that a higher pH milieu in the stomach enhances chances of Aeromonas intestinal colonization. The findings that Enterobacteriaceae are the most common concurrent pathogens for AIPMB in other reports and ours further support the gastrointestinal tract as the most likely portal of entry for Aeromonas leading to bacteremia [12], [13], [14].

Of all bacteremia cases, a higher proportion of polymicrobial bacteremia is reported in cancer patients compared with their non-cancer counterparts [24], [25]. Of note, one study found polymicrobial bloodstream infection in 14% of 2340 patients with an underlying malignancy and an episode of nosocomial bloodstream infection [1]. Neutropenia and disruption of the digestive mucosal barrier caused by antineoplastic therapy, surgery or hypoxia in cancer patients enables the invasion of various bacteria, especially from the gut and oropharynx [1], [26]. In agreement with these findings, 12 of the 28 cancer patients in the present study had abdominal surgery, eight had received antineoplastic therapy, two had received radiotherapy and six had septicemia shortly before AIPMB occurred.

Cirrhosis plays an important role in the pathogenesis of AIPMB as it leads to many alterations in the immune system, including decreased reticuloendothelial phagocytic activity, deficient ascetic fluid opsonic activity and qualitative neutrophil dysfunction [27], [28], [29], [30]. Cirrhosis-associated portal hypertension could alter intestinal permeability as a result of intestinal congestion, edema and local hypoxia [31], [32], [33], [34], [35], [36].

In this study, >85% of Aeromonas isolates in both community-acquired and healthcare-associated AIPMB were susceptible to gentamicin, amikacin, ceftriaxone, ceftazidime, cefpirome, aztreonam, piperacillin/tazobactam, imipenem and ciprofloxacin. The similarity in antibiotic susceptibility suggests that the bloodstream-invasive Aeromonas in healthcare-associated infections existed in the gastrointestinal tracts of affected patients before hospitalization and were not acquired from the institutional environment [8]. The difference in concurrent pathogens in AIPMB between healthcare-associated and community-acquired patients might result from the alteration of microbes that inhabit the patients’ bowel after hospitalization [37] and which then invade the bloodstream leading to the development of bacteremia. Non-Enterobacteriaceae from hospital environments, such as non-fermentative Gram-negative bacilli or Gram-positive bacteria, can colonize patients’ gastrointestinal tracts while they are hospitalized.

One limitation of this study was that the Aeromonas isolates could not be identified to species level, as neither automated system (i.e., the API-20NE, Vitek II system and BD-Phoenix system) nor conventional biochemical reactions were ideal for this task.

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5. Conclusions 

The most common underlying diseases/conditions in patients with AIPMB were solid tumors, liver cirrhosis and gastric acid suppressant therapy. Although Enterobacteriaceae were the most common concurrent pathogens for AIPMB, no significant difference in antibiotic susceptibility was found between Aeromonas isolates in healthcare-associated and community-acquired AIPMBs.

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Acknowledgments 

The authors are indebted to staff at the clinical microbiology laboratories at the Tzu Chi Hospitals for their meticulous assistance with the collection of microbiological and susceptibility information.

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 Conflict of interest: none.

PII: S1016-3190(11)00093-0

doi:10.1016/j.tcmj.2011.09.003

Tzu Chi Medical Journal
Volume 23, Issue 4 , Pages 119-122, December 2011

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