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Journal of Clinical Microbiology, April 2009, p. 1234-1237, Vol. 47, No. 4
0095-1137/09/$08.00+0     doi:10.1128/JCM.00155-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Prospective Nationwide Study of Aeromonas Infections in France

Brigitte Lamy,^1,2,3* Angeli Kodjo,^3,4 the colBVH Study Group,² Frédéric Laurent,^2,3,5,6

Laboratoire de Biologie, Centre Hospitalier du Bassin de Thau, Sète, France,¹ Collège de Bactériologie, Virologie et Hygiène des Hôpitaux Généraux, Le Chesnay, France,² Groupe d'Étude Français sur les Aeromonas (GFA), Lyon, France,³ UMR 5557 Ecologie Microbienne, Université Lyon 1, Ecole Nationale Vétérinaire de Lyon, Lyon, France,⁴ Hospices Civils de Lyon, Laboratoire de Bactériologie de l'Hôpital de la Croix-Rousse, Lyon, France,⁵ INSERM U851, Université de Lyon, Lyon, France⁶

Received 24 January 2009/ Accepted 17 February 2009

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We report a systematic prospective multicenter nationwide study of clinical Aeromonas infections in France. During 6 months (May to October 2006), 78 cases of aeromonosis were reviewed for risk factors and clinical, microbiological, and antimicrobial susceptibility data. They included wound infections (44%), bacteremia (26%), enteritis (19%), respiratory tract infections (6%), and miscellaneous (5%) infections.

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Aeromonas species are opportunistic pathogens involved in various types of infections. Previously published epidemiological studies are usually limited to one type of infection, and global epidemiological studies are scarce. In Europe, the studies were rare, retrospective, and restricted to a few cases and/or they involved lengthy study periods with epidemiological changes during their course (3, 24, 29, 34). To complete these epidemiological data, we present an overview of the characteristics of all types of Aeromonas infections occurring in France during a short defined period including warm months based on a prospective multicenter nationwide study (70 hospitals).

During 6 months (May to October 2006), all patients from whom an aeromonad was isolated were included. Cases were categorized as definite, possible, and doubtful infections, based on data prospectively collected from standardized records. Definite and possible infections included isolation of an Aeromonas bacterium either from a sterile site or in pure culture (definite infection) or in mixed culture (possible infection), clinical and biological signs of infection, exclusion of other etiologies, and decision to treat. Doubtful infection included isolation of an Aeromonas bacterium, no clinical signs of infection, and decision not to treat. Cutaneous and pulmonary exposure to a potential Aeromonas-contaminated environment (water and soil) was recorded from the medical history. Community-acquired infection was defined by Aeromonas culture from a first specimen obtained less than 48 h after admission. Strains were identified with partial sequence analysis of the rpoB gene, including sequences of all 19 known Aeromonas species type strains, as reported elsewhere (20, 22). Antimicrobial susceptibility was tested with the disk diffusion method on Mueller-Hinton agar according to the guidelines of the Comité de l'antibiogramme de la Société Francaise de Microbiologie (6). Qualitative variables were compared with the chi-square test or Fisher's exact test where appropriate.

Out of the 99 included patients, 78 (79%), were considered infected. The infection was nosocomial in six cases (7%). Seventy of the 84 Aeromonas isolates recovered from these 78 patients were studied. The disease distribution, patient characteristics, and risk factors are shown in Table 1. Differences in age, sex ratio, comorbidity, and environmental exposure frequencies were noted across types of infection. Interestingly, wound and skin soft-tissue infections (SSTI), followed by bacteremia, were the most prevalent infections, as reported elsewhere (9).

View this table: [in this window] [in a new window]

TABLE 1. Clinical characteristics, risk factors, and microbiological characteristics for Aeromonas infections in France

Wound infections and SSTI (34 cases) consisted of purulent wound infection (25 cases, 74%) and soft-tissue abscesses (nine cases, 26%). These infections mainly occurred in otherwise healthy patients (88%), among whom young men predominated. Rates of trauma and of environmental exposure concomitant with the trauma (both >90%) were among the highest reported (10, 13, 16, 31). Injuries with water exposure (15 cases) involved only freshwater, as reported elsewhere (31), and resulted mainly from leisure activities (14 cases). Injuries with soil exposure (15 cases) involved penetrating wounds (five cases) or road accidents (10 cases). These characteristics are in keeping with the literature (9, 13, 16). No cases were related to leech therapy. This occasional etiology, related to reconstructive surgery, could be underrepresented in our series because this type of surgery is underpracticed in our participating hospitals (9, 30). Finally, wound infections and SSTI required surgical or antimicrobial treatment in 23 (68%) and 29 (85%) of the 34 cases, respectively. Interestingly, initial antibiotic treatment was inappropriate for 18 of the 29 patients (62%).

Patients with bacteremia (20 cases) showed characteristics that differed somewhat from published data (7, 14, 18, 23, 29). Females were as numerous as males. Six (30%) patients had no underlying health disorders, a rate higher than that reported elsewhere (7, 12, 14, 17, 23). Among these, very elderly patients predominated (five patients of >80 years and four patients of >90 years). These noteworthy features suggest, like the results from the work of Llopis et al. (24), that Aeromonas bacteremia is associated with very elderly and otherwise healthy patients and may become more frequent as Western populations age. The distribution of comorbidities associated with Aeromonas bacteremia (Table 1) was similar to that reported in the United States and Europe (14, 24, 29) but different from that reported in Asia (7, 18, 23, 37). In Asia, the higher prevalence of liver and biliary diseases combined with the higher frequency of Aeromonas intestinal carriage could explain the observed difference from Western countries (4, 7, 36). Gut was the suspected source in all of our patients. Biliary tract disease was frequent (7 cases of 20, 35%). This disease should therefore be sought in cases of Aeromonas bacteremia. In contrast to previous reports, Aeromonas bacteremia was never related to wound and SSTI in our series (18, 23, 24). The overall fatality rate was 35% (7 patients of 20). Interestingly, this rate was 17% (one of six) in the group of elderly patients with no comorbidity and 43% (6 of 14) in the group of younger patients with comorbidities.

Aeromonas species as a causative agent of gastroenteritis remain controversial due to digestive carriage and weak evidence of enteropathogenicity (13, 36). Still, our series comprised 15 cases of gastroenteritis, suggesting that Aeromonas-associated diarrhea is rare in France or does not require hospital management. Malignancy was present in six (40%) cases (Table 1). This high rate could be related to the population studied, namely, hospitalized patients. However, higher digestive tract colonization by Aeromonas and a subsequently higher risk of diarrhea have been suggested in neutropenic patients with hematologic malignancies, although our series dealt instead with solid malignancies (32).

Our series included five cases of respiratory tract infection (RTI), with clinical severity, a preponderance of males, comorbidity, and/or massive aquatic environmental exposure. Three of our patients were near-drowning victims, a frequent risk factor (2). The involvement of Aeromonas species recovered from sputum remains difficult to establish, particularly when other pathogens are found. However, several cases of severe infection have been reported with Aeromonas species in mixed culture (2). Given that Aeromonas is now recognized as a respiratory tract pathogen, although rarely encountered (2, 11, 13, 15, 25, 26, 28, 33), our cases with mixed culture were categorized as "possible infection" to better reflect the RTI frequency.

Finally, four specific infections included ocular infection, hepatobiliary infection, urinary tract infection, and peritonitis with mesenteric ulcer perforation, all occasionally reported (4, 5, 13, 27).

Sixty-nine (99%) of the 70 Aeromonas isolates analyzed belonged to "clinically relevant" Aeromonas species (Table 1) (8, 13). The species isolated here were similar to those reported elsewhere (13), although their distribution differed somewhat (1, 19), probably due to the identification method used, use of an updated taxonomy, and the geographical location of the study. Aeromonas hydrophila was less frequent in bacteremia (P = 0.006) and more frequent in wound infections (P = 0.0008) than in other infections. Aeromonas caviae was less prevalent in wound infections (P = 0.0077) and more prevalent in bacteremia (P = 0.03) than in other infections. Aeromonas veronii was not associated with a particular type of infection. Culture yielded polymicrobial growth in 33 (42%) infected patients (from 30% for bacteremia to 80% for RTI [Table 1]), data in keeping with previous reports (7, 16-18, 23, 24, 29, 31, 35). In seven samples (9% of samples), more than one strain of Aeromonas was isolated, mainly from patients with wound infections or SSTI, suggesting an exposure to an environment with high Aeromonas diversity (21). Such cases might be underestimated, as microbiologists may not systematically search for mixed aeromonad cultures.

The analysis of antimicrobial susceptibility (Table 2) showed a low rate of co-amoxiclav susceptibility, which is of concern because wound infections are often empirically treated with this drug (in this study, 14 of the 29 wound cases [47%] treated with antibiotics). Given the high rate of mixed infections, the lack of specific clinical signs of Aeromonas infection, the current susceptibility data, and the previous reports, the most active empirical treatments would consist of a broad-spectrum cephalosporin or a fluoroquinolone, combined with gentamicin or amikacin in cases of severe infection (18).

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TABLE 2. Susceptibilities of Aeromonas isolates recovered from infected patientsa

In summary, we report a detailed overview of Aeromonas infections encountered in a temperate European country during the warm months, with an update on antimicrobial susceptibility that should be useful for patient management.

 
We thank all the members of the colBVH study group who participated in this study (all in France): F. Carmagnol (Cannes), E. Chachaty (Institut Gustave Roussy), C. Alba-Sauviat (Chaumont), C. Auvray (Charleville-Mézières), D. Barraud (Gonesse), Z. Benseddik (Chartres), A. Bertrou (Carcassone), F. Bessis (Cherbourg), H. Biessy (La Rochelle), V. Blanc (Antibes-Juan-les-pins), Y. Boucaud-Maitre (Lyon), P. Brunet and A. Michel (Marseille), B. Cancet (Villeneuve/Lot), J. Carrere (Hyères), A. Cecille (Digne-les-bains), G. Chambreuil (La Roche/Yon), P. Chantelat (Vesoul), H. Chardon (Aix en Provence), C. Charrel (Salon de Provence), H. De Montclos (Bourg-en-Bresse), J. W. Decousser (Dourdan; Rambouillet), J. M. Delarbre and A. Gravey (Mulhouse), D. Deligne (Remiremont), C. Denoix (La Réunion), J. Deregnaucourt (Paris [H. L. Bellon]), F. Desroys du Roure (Chatellerault), S. Dubourdieu (Gisors), Z. El Harrif (Libourne), C. Eloy (Troyes), A. Evers (Annonay), C. Febvre (Montbéliard), D. Fevre (Vienne), S. Gabriel (Monaco), M. J. Galanti (Coulommiers), E. Garnotel (Marseille [HIA Laveran]), M. Gavignet (Lavaur), F. Geffroy (Quimper), G. Grise (Elbeuf-Louviers), I. Gros (St. Denis), I. Hermes (St.-Malo), J. Heurte (Beauvais), E. Heusse (Bayeux), D. Jan (Laval), E. Jaouen (Sablé/Sarthe), S. Laluque (Montluçon), R. Lamarca (Narbonne), B. Lamy (Sète), E. Laurens (Belfort), A. Le Coustumier (Cahors), E. Lecaillon (Perpignan), C. Lemble (Selestat), M. Leneveu (Poissy; St.-Germain), S. Leotard (Grasse), M. N. Letouzey (Villefranche/Saone), C. Malbrunot (Corbeil-Essonnes), O. Menouni (Montceau-les-Mines), A. Morel (Le Havre), C. Olive (Fort de France), B. Pangon (Versailles), J. G. Paul (Boulogne/Mer), J. M. Perez (Pte à Pitre), P. Pouedras (Vannes), D. Pressac (Tulle), R. Sanchez (Périgueux), Y. Scat (Pontivy), A. Secher (Dreux), J. Semon (Chalon sur Saone), D. Simeon (Langres), C. Simonin (Macon), J. P. Thellier (Château Thierry), B. Tourand (Alès), A. Vachée (Roubaix), C. Varache (Le Mans), J. Vaucel (St.-Brieux), A. C. Vautrin (St.-Etienne), A. Verhaeghe (Dunkerke), M. Villemain (Aurillac), and L. Villeneuve (Aubagne).

This work was supported by Association des Biologistes de l'Ouest.

We thank L. Marjolet, E. Borges, L. Loiseau, and F. Maurin for technical assistance and H. Marchandin for helpful comments. The manuscript has been checked for English-language accuracy by D. Young.

 
* Corresponding author. Mailing address: Laboratoire de Biologie, Centre Hospitalier du Bassin de Thau, Boulevard Camille Blanc, 34207 Sète, France. Phone: (33) (0) 4-67-46-57-82. Fax: (33) (0) 4-67-46-59-84. E-mail: blamy{at}ch-bassindethau.fr

Published ahead of print on 25 February 2009.

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Journal of Clinical Microbiology, April 2009, p. 1234-1237, Vol. 47, No. 4
0095-1137/09/$08.00+0     doi:10.1128/JCM.00155-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Lamy, B. Articles by Laurent, F. Search for Related Content PubMed PubMed Citation Articles by Lamy, B. Articles by Laurent, F.