Aeromonas spp. and traveler's diarrhea: clinical features and antimicrobial resistance. (Research).Traveler's diarrhea Traveler's Diarrhea Definition The occurrence of multiple loose bowel movements in someone traveling to an area outside their usual surroundings (usually from temperate industrialized regions to tropical areas), is known as Traveler's diarrhea (TD). is the most common health problem of international travelers. We determined the prevalence of Aeromonas spp Aeromonas spp Microbiology A genus of gram-negative, facultatively anaerobic, nonspore-forming bacilli, which have been isolated from various foods, including dairy products, meats and vegetable; Aeromonas . associated with traveler's diarrhea and analyzed the geographic distribution, clinical features, and antimicrobial susceptibility. Aeromonas spp. were isolated as a cause of traveler's diarrhea in 18 (2%) of 863 patients. A. veronii biotype biotype /bio·type/ (bi´o-tip) 1. a group of individuals having the same genotype. 2. any of a number of strains of a species of microorganisms having differentiable physiologic characteristics. sobria was isolated in nine patients, A. caviae in seven patients, and A. jandaei and A. hydrophila in one patient each. Aeromonas spp. were isolated with a similar prevalence in Africa, Latin America, and Asia. Watery and persistent diarrhea, fever, and abdominal cramps were common complaints. All strains were resistant to ampicillin ampicillin (ăm'pĭsĭl`ĭn), a penicillin-type antibiotic that is effective against both gram-negative microorganisms and gram-positive microorganisms such as Escherichia coli. ; showed variable resistance to chloramphenicol chloramphenicol (klōr'ămfĕn`əkŏl'), antibiotic effective against a wide range of gram-negative and gram-positive bacteria (see Gram's stain). It was originally isolated from a species of Streptomyces bacteria. , tetracycline tetracycline (tĕ'trəsī`klēn), any of a group of antibiotics produced by bacteria of the genus Streptomyces. They are effective against a wide range of Gram positive and Gram negative bacteria, interfering with protein , and cotrimoxazole; and were susceptible to cefotaxime, ciprofloxacin ciprofloxacin /cip·ro·flox·a·cin/ (sip?ro-flok´sah-sin) a synthetic antibacterial effective against many gram-positive and gram-negative bacteria; used as the hydrochloride salt. cip·ro·flox·a·cin n. , and nalidixic acid nalidixic acid /nal·i·dix·ic ac·id/ (nal-i-dik´sik) a synthetic antibacterial agent used in the treatment of genitourinary infections caused by gram-negative organisms. na·li·dix·ic acid n. . The persistence of symptoms made antimicrobial treatment necessary. ********** Traveler's diarrhea is the main infectious disease Infectious disease A pathological condition spread among biological species. Infectious diseases, although varied in their effects, are always associated with viruses, bacteria, fungi, protozoa, multicellular parasites and aberrant proteins known as prions. reported in persons traveling abroad. Among the microorganisms responsible, bacteria represent approximately 61% (1). Enterotoxigenic Escherichia coli Enterotoxigenic Escherichia Coli (ETEC) is a type of Escherichia coli that can cause Traveler's diarrhea. A number of pathogenic isolates are termed ETEC, but the main hallmarks of this type of bacteria are expression of one or more enterotoxins and presence of , enteroaggregative E. coli E. coli: see Escherichia coli. E. coli in full Escherichia coli Species of bacterium that inhabits the stomach and intestines. E. coli can be transmitted by water, milk, food, or flies and other insects. , and Shigella shigella Any of the rod-shaped bacteria that make up the genus Shigella, which are normal inhabitants of the human intestinal tract and can cause dysentery, or shigellosis. Shigellae are gram-negative (see gram stain), non-spore-forming, stationary bacteria. S. spp. are the most common bacteria involved (1,2). Other bacteria that cause diarrhea, such as Salmonella, Campylobacter Campylobacter Genus of gram-negative spiral-shaped bacteria infecting mammals. Many species, especially C. fetus, cause miscarriage in sheep and cattle. C. jejuni is a common cause of food poisoning. Sources include meats (particularly chicken) and unpasteurized milk. , Yersinia Yersinia A genus of bacteria in the Enterobacteriaceae family. The bacteria appear as gram-negative rods and share many physiological properties with related Escherichia coli. Of the 11 species of Yersinia, Y. pestis, Y. enterocolitica, and Y. , Aeromonas, and Plesiomonas spp., are isolated less often (1). The genus Aeromonas has high diversity: at least 16 DNA hybridization groups are recognized (3). Among these genospecies, A. hydrophila, A. caviae, and A. veronii biotype sobria are considered of clinical significance (4,5). The spectrum of infectious diseases caused by Aeromonas species includes gastrointestinal infections as well as extraintestinal infections such as cellulitis Cellulitis Definition Cellulitis is a spreading bacterial infection just below the skin surface. It is most commonly caused by Streptococcus pyogenes or Staphylococcus aureus. , wound infections, septicemia septicemia (sĕptĭsē`mēə), invasion of the bloodstream by virulent bacteria that multiply and discharge their toxic products. The disorder, which is serious and sometimes fatal, is commonly known as blood poisoning. , urinary tract infections, and hepatobiliary and ear infections, among others (6). Although healthy carriers of Aeromonas spp. have been described, several case-control studies have shown that these bacteria cause diarrhea (6). With the incorporation of genotypic techniques, identification of Aeromonas to species level has improved (7). The main objective of this study was to determine the prevalence of Aeromonas spp. as a cause of traveler's diarrhea and to analyze the species' geographic distribution, clinical features, and susceptibility to antimicrobial agents. Methods Patients A total of 863 patients with traveler's diarrhea were recruited from the Tropical Medicine Unit of the Hospital Clinic of Barcelona, Spain, during the period January 1999-December 2001. All patients completed an epidemiologic questionnaire; their clinical history was taken, and a physical examination was performed. Traveler's diarrhea was defined as the occurrence of three or more episodes of watery stool within a 24-hour period, with or without other symptoms, or the occurrence of unformed stools accompanied by one of the following: vomiting, nausea, abdominal cramps, fever, chills, prostration prostration /pros·tra·tion/ (pros-tra´shun) extreme exhaustion or lack of energy or power. heat prostration see under exhaustion. pros·tra·tion n. , or tenesmus tenesmus /te·nes·mus/ (te-nez´mus) straining, especially ineffectual and painful straining at stool or urination.tenes´mic te·nes·mus n. . Persistent diarrhea was defined as that of > 14 days' duration. Microbiologic Tests A stool sample was collected, sent to the Laboratory of Clinical Microbiology, and processed for bacterial, viral, and parasitologic studies. To isolate Aeromonas spp., blood agar supplemented with ampicillin and a selective media, CIN CIN cervical intraepithelial neoplasia. Cervical intraepithelial neoplasia (CIN) A term used to categorize degrees of dysplasia arising in the epithelium, or outer layer, of the cervix. (cefsulodin-irgasan-novobiocin) agar, were used. After incubation at 37[degrees]C for 24-48 hours, an oxidase test was performed on the colonies compatible with bacilli bacilli /ba·cil·li/ (bah-sil´i) plural of bacillus. bacilli see bacillus. . Biochemical criteria were used to identify Aeromonas. Identification of the species was performed by 16S rDNA--restriction fragment length polymorphism as previously described (7,8). The biotype of A. veronii strains was identified on the basis of a positive reaction to arginine arginine (är`jənĭn), organic compound, one of the 20 amino acids commonly found in animal proteins. Only the l-stereoisomer participates in the biosynthesis of proteins. dihydrolase and negative response to bilis-esculin hydrolysis hydrolysis (hīdrŏl`ĭsĭs), chemical reaction of a compound with water, usually resulting in the formation of one or more new compounds. and production of ornithine decarboxylase (9). Susceptibility Testing Antimicrobial susceptibility tests were performed by using an agar disk diffusion method advocated by the National Committee for Clinical Laboratory Standards (10). Antimicrobial disks (ampicillin 10 [micro]g; cefotaxime 30 [micro]g; chloramphenicol 30 [micro]g; ciprofloxacin 5 [micro]g; nalidixic acid 30 [micro]g; tetracycline 30 [micro]g; and trimethoprim-sulfamethoxazole 1.25/23.75 [micro]g) were obtained from Becton Dickinson (Cockeysville, MD). E. coli ATCC ATCC American Type Culture Collection, see there 25922 and Pseudomonas aeruginosa ATCC 27853 were used as quality-control strains. Results Distribution and Geographic Origin of Species Causing Traveler's Diarrhea Aeromonas spp. were isolated as a cause of traveler's diarrhea in 18 (2%) of 863 patients. A. veronii biotype sobria was isolated in nine patients, A. caviae in seven patients, and A. jandaei and A. hydrophila in one patient each (Table 1). In three of these patients, another enteropathogen en·ter·o·path·o·gen n. An organism that is capable of producing intestinal disease. en  ter·o·path was also found: in one patient who had traveled
to Mexico, Shigella sonnei was isolated together with A. veronii; in
another patient traveling to India, Giardia lamblia was detected
together with A. veronii; in the third patient, who had traveled to
Thailand, Salmonella Typhimurium was found with A. veronii. The
frequency of Aeromonas spp. as a cause of traveler's diarrhea was
similar in patients returning from Africa (1.7%), Latin America (1.8%),
and Asia (2.3%) (Table 1).Clinical Features The signs and symptoms of Aeromonas enteritis enteritis (ĕn'tərī`tĭs), inflammation of the gastrointestinal tract. Acute enteritis is not usually serious except in infants and older people, in whom the accompanying diarrhea can cause dehydration through the loss of fluids. in these 18 patients are summarized in Table 2. Sixteen of the 18 patients had watery diarrhea; these were the cases associated with A. veronii biotype sobria and A. caviae. The patients with enteritis caused by A. hydrophila and A. jandaei had loose stools. Fifty percent of the patients had fever and abdominal cramps, whereas nausea and vomiting Nausea and Vomiting Definition Nausea is the sensation of being about to vomit. Vomiting, or emesis, is the expelling of undigested food through the mouth. were uncommon complaints. Gross blood was observed in the stools of one patient, but this could be attributed to the S. sonnei isolated in the same stool. In 9 of the 18 patients, diarrhea was persistent. Antimicrobial Susceptibility The antimicrobial susceptibility of Aeromonas spp. isolates causing traveler's diarrhea is shown in Table 3. All strains were resistant to ampicillin but susceptible to cefotaxime, ciprofloxacin, and nalidixic acid. The susceptibility to chloramphenicol, tetracycline, and trimethoprim-sulfamethoxazole varied. Some 66.6% of A. veronii biotype sobria strains and 71.4% of A. caviae strains were susceptible to chloramphenicol; 55.6% of A. veronii biotype sobria strains and 71.4% of the A. caviae strains were susceptible to tetracycline; and 77.8% of A. veronii biotype sobria and 100% of A. caviae were susceptible to trimethoprim-sulfamethoxazole. Treatment While travelling, two patients received treatment, amoxicillin amoxicillin /amox·i·cil·lin/ (ah-mok?si-sil´in) a semisynthetic derivative of ampicillin effective against a broad spectrum of gram-positive and gram-negative bacteria. a·mox·i·cil·lin n. in one case and amoxicillin plus clavulanic acid in the other. Patients with persistent diarrhea were treated with the following antibiotics: norfloxacin (one patient), ciprofloxacin (six patients), and trimethoprim-sulfamethoxazole (two patients); all recovered. Discussion In this study we describe the prevalence of different types of Aeromonas species associated with traveler's diarrhea in a cohort of travelers to a variety of tropical and subtropical sub·trop·i·cal adj. Of, relating to, or being the geographic areas adjacent to the Tropics. subtropical Adjective of the region lying between the tropics and temperate lands countries. In contrast, other published studies have often been selective in terms of the types of travelers, geographic areas visited, or attempts to isolate specific microorganisms with the aim of testing antibiotic efficiency. In our study, Aeromonas spp. were isolated in 18 (2%) of 863 patients with traveler's diarrhea. A. veronii biotype sobria and A. caviae were the most frequently isolated species. These findings agree with the results of Hanninen et al. (11), who reported that these were the most common Aeromonas spp. associated with traveler's diarrhea in tourists traveling to Morocco. Likewise, Yamada et al. (12) found that A. veronii biotype sobria was the Aeromonas species most frequently implicated im·pli·cate tr.v. im·pli·cat·ed, im·pli·cat·ing, im·pli·cates 1. To involve or connect intimately or incriminatingly: evidence that implicates others in the plot. 2. as a cause of traveler's diarrhea in Japanese travelers returning from unindustrialized countries. In our study, the geographic distribution of Aeromonas species did not favor any predominant area: species were isolated with a similar prevalence in Africa, Latin America, and Asia. However, all four species (A. veronii biotype sobria, A. caviae, A. jandaei, and A. hydrophila) were isolated from patients returning from India. In India, Aeromonas spp. has been identified as an enteric enteric /en·ter·ic/ (en-ter´ik) within or pertaining to the small intestine. en·ter·ic adj. 1. Of, relating to, or within the intestine. 2. pathogen in 1.8% of patients with diarrhea (13). In a recent study performed in Dhaka (Bangladesh), Aeromonas spp. were significantly associated with diarrhea, similar to occurrences in other countries (14-17). In our study, 3 (16.7%) of the Aeromonas isolates were detected together with other enteropathogens. This situation allowed us to consider that the symptoms we observed in the patients with traveler's diarrhea associated with Aeromonas spp. were due to the presence of this Aeromonas organisms. In our study, watery stools, fever, and abdominal cramps were the most common symptoms, which is consistent with other reports (11,18). Albert et al. (18) suggested that isolates of Aeromonas spp. positive for both the alt and ast genes, which encode enterotoxins, were associated with watery diarrhea but that isolates positive only for the alt gene were associated with loose stools. Fifty percent of the patients with Aeromonas spp. enteritis had persistent diarrhea. Chronic diarrhea lasting more than 1 year caused by A. caviae has been reported (2). A direct link between drinking water and food contaminated with Aeromonas spp. and gastrointestinal disease has been demonstrated (19). Patients with prolonged enteritis required treatment. A quinolone was the drug of choice, although increased occurrence of quinolone-resistant Aeromonas spp. strains has been reported in industrialized in·dus·tri·al·ize v. in·dus·tri·al·ized, in·dus·tri·al·iz·ing, in·dus·tri·al·iz·es v.tr. 1. To develop industry in (a country or society, for example). 2. countries (20,21). Regarding the [beta]-lactam antibiotics, Aeromonas spp. strains analyzed in this study were, as expected, uniformly resistant to ampicillin, whereas third-generation cephalosporins Cephalosporins Definition Cephalosporins are medicines that kill bacteria or prevent their growth. Purpose Cephalosporins are used to treat infections in different parts of the body—the ears, nose, throat, lungs, sinuses, and , such as cefotaxime, showed good activity. These results are in accordance with those reported by other authors, showing that third-generation cephalosporins are active against Aeromonas spp. (2,22). The percentage of strains with resistance to chloramphenicol, tetracycline, or trimethoprim-sulfamethoxazole ranged from 22.9% to 45%. These levels of resistance are likely related to the extensive use of these antimicrobial agents in unindustrialized countries. In summary, A. veronii biotype sobria and A. caviae are the Aeromonas species most frequently associated with traveler's diarrhea; watery diarrhea, fever, and abdominal cramps are the predominant clinical features. The persistence of symptoms makes the use of antimicrobial treatment necessary.
Table 1. Species and geographic distribution of clinical isolates
of Aeromonas spp. causing traveler's diarrhea
A. veronii biotype
Geographic area sobria (n=9) A. caviae (n=7)
Guatemala 1 1
India 2 1 (a)
Iran 1
Kenya 1
Mali/Burkina Faso 1
Mexico 2 (b)
Nicaragua 1
Paraguay 1
Sahara 1
Senegal 2
Thailand 1
Geographic area A. jandaei (n=1) A. hydrophila (n=1)
Guatemala
India 1 (a) 1
Iran
Kenya
Mali/Burkina Faso
Mexico
Nicaragua
Paraguay
Sahara
Senegal
Thailand
(a) This patient traveled to India and Nepal.
(b) One traveler also visited Guatemala.
Table 2. Clinical features of patients with traveler's diarrhea
associated with Aeromonas spp.
No. of patients with symptoms/
total patients (n=18)
A. veronii A.
Sign or symptom biotype sobria caviae Overall (a)
Watery diarrhea 9/9 7/7 16/18
Abdominal cramps 6/9 3/7 10/18
Persistent diarrhea 3/9 5/7 9/18
Fever 6/9 3/7 10/18
Nausea, vomiting, or both 2/9 0/7 3/18
Gross blood in stools 1 (b)/9 0/7 1/18
(a) Also includes A. hydrophila and A. jandai.
(b) In this patient, a Shigella sonnei strain was also isolated.
Table 3. Antimicrobial susceptibility of Aeromonas spp. causing
traveler's diarrhea
No. of isolates showing susceptibility
A. veronii biotype
Antimicrobial agent sobria (n=9) A. caviae (n=7)
Ampicillin 0 0
Cefotaxime 9 7
Chloramphenicol 6 5
Ciprofloxacin 9 7
Nalidixic acid 9 7
Tetracycline 5 5
Trimethoprim/ 7 7
sulfamethoxazole
This work was partially supported by grant FIS FIS n abbr (BRIT) (= Family Income Supplement) → ayuda estatal familiar 00/0997 of Fondo de Investigaciones Sanitarias. References (1.) Gascon Gascon inhabitant of Gascony, France; people noted for their bragging. [Fr. Hist.: NCE, 1049] See : Boastfulness J, Vila J, Valls ME, Ruiz L, Vidal J, Corachan M, et al. Etiology of traveller's diarrhea in Spanish travellers to developing countries. Eur J Epidemiol 1993;9:217-23. (2.) Rautelin H, Hanninen ML, Sivonen A, Turunen U, Valtonen V. Chronic diarrhea due to single strain of Aeromonas caviae. Eur J Clin Microbiol Infect Dis 1995;14:51-4. (3.) Figueras MJ, Guarro J, Martinez-Murcia AJ. Clinical relevant Aeromonas species. Clin Infect Dis 2000;30:988-9. (4.) Janda JM. Recent advances in the study of the taxonomy, pathogenicity, and infectious syndromes associated with the genus Aeromonas. Clin Microbiol Rev 1991;4:397-410. (5.) Janda JM, Abbott SL. Evolving concepts regarding the genus Aeromonas: an expanding panorama of species, disease presentations, and unanswered questions. Clin Infect Dis 1998;27:332-44. (6.) Janda JM, Abbott SL, Morris JG Jr. Aeromonas, Plesiomonas, and Edwarsiella. In: Blaser MJ, Smith PD, Ravdin JI, Greenberg HB, Guerrant RL, editors. Infections of gastrointestinal tract. New York: Raven Press; 1995. (7.) Borrell N, Acinas SG, Figueras MJ, Martinez-Murcia AJ. Identification of Aeromonas clinical isolates by restriction fragment length polymorphism restriction fragment length polymorphism n. Abbr. RFLP Intraspecies variations in the length of DNA fragments generated by the action of restriction enzymes and caused by mutations that alter the sites at which these enzymes act, changing of PCR-amplified 16S rDNA genes. J Clin Microbiol 1997;35:1671-4. (8.) Figueras M J, Soler L, Chacon MR, Guarro J, Martinez-Murcia AJ. Extended method for discrimination of Aeromonas spp. by 16S rDNA-RFLP analysis. Int J Syst Evol Microbiol 2000;50:2069-73. (9.) Borrell N, Figueras M J, Guarro J. Phenotypic identification of Aeromonas genomospecies from clinical and environmental sources. Can J Microbiol 1998;44:7-12. (10.) National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial susceptibility testing: approved standard M 100-S 11. Wayne (PA): The Committee; 2001. (11.) Hanninen ML, Salmi S, Mattila L, Taipalinen R, Siitonen A. Association of Aeromonas spp. with travellers' diarrhoea in Finland. J Med Microbiol 1995;42:26-31. (12.) Yamada S, Matsushita S, Dejsirilert S, Kudoh Y. Incidence and clinical symptoms of Aeromonas-associated traveller's diarrhea in Tokyo. Epidemiol Infect 1997; 119:121-6. (13.) Deodhar LP, Saraswathi K, Varudkar A. Aeromonas spp. and their association with human diarrheal disease. J Clin Microbiol 1991;29:853-6. (14.) Albert JM, Faruque ASG ASG Assign ASG Allen Systems Group (Naples, FL) ASG Abu Sayyaf Group (terrorist group) ASG Associated Student Government ASG Area Support Group ASG Adaptive Services Grid ASG Assistant Secretary General , Faruque SM, Sack RB, Mahalanabis D. Case-control study of enteropathogens associated with childhood diarrhea in Dhaka, Bangladesh. J Clin Microbiol 1999;37:3458-64. (15.) Begue RE, Castellares G, Hayashi KE, Ruiz R, Meza R, English CK, et al. Diarrheal disease in Peru after the introduction of cholera. Am J Trop Med Hyg 1994;51:585-9. (16.) Kuhn I, Albert MJ, Ansaruzzaman M, Bhuiyan NA, Alabi SA,. Islam MS, et al. Characterization of Aeromonas spp. isolated from humans with diarrhea, from healthy controls, and from surface water in Bangladesh. J Clin Microbiol 1997;35:369-73. (17.) Ogunsanya TI, Rotimi VO, Adenuga A. A study of the aetiological AE`ti`o`log´ic`al a. 1. Pertaining to ætiology; assigning a cause. Adj. 1. aetiological - of or relating to the philosophical study of causation aetiologic, etiologic, etiological 2. agents of childhood diarrhea in Lagos, Nigeria. J Med Microbiol 1994;40:10-4. (18.) Albert MJ, Ansaruzzaman M, Talukder KA, Chopra AK, Kuhn I, Rahman M, et al. Prevalence of enterotoxin enterotoxin /en·tero·tox·in/ (en´ter-o-tok?sin) 1. a toxin specific for the cells of the intestinal mucosa. 2. a toxin arising in the intestine. 3. genes in Aeromonas spp. isolated from children with diarrhea, healthy controls, and the environment. J Clin Microbiol 2000;38:3785-90. (19.) Joseph SW. Aeromonas gastrointestinal disease: a case study in causation? In: Austin B, Altwegg M, Gosling PJ, Joseph S, editors. The genus Aeromonas. New York: John Wiley & Sons; 1996. (20.) Goni-Urriza M, Pineau L, Capdepuy M, Roques Roques is the name or part of the name of several communes in France:
(21.) Vila J, Marco F, Soler L, Chacon M, Figueras MJ. In vitro antimicrobial susceptibility of clinical isolates of Aeromonas caviae, Aeromonas hydrophila and Aeromonas veronii biotype sobria. J Antimicrob Chemother 2002;49:701-2. (22.) Motyl MRG MRG Merge MRG Minority Rights Group International MRG Mad River Glen (Vermont) MRG Mouvement des Radicaux de Gauche (French: Left Radical Movement) MRG Manyetik Rezonans Görüntüleme , MacKinley G, Janda JM. In vitro susceptibilities of Aeromonas hydrophila, Aeromonas sobria, and Aeromonas caviae to 22 antimicrobial agents. Antimicrob Agents Chemother 1985;28:151-3. Address for correspondence: Jordi Vila, Laboratori de Microbiologia, Institut d'Infeccions i Immunologia, Institut d'Investigacions Biomediques August Pi i Sunyer, Facultat de Medicina, Universitat de Barcelona, Villarroel, 170; 08036 Barcelona, Spain; fax: 34.93.2279372; email: vila@medicina.ub.es Jordi Vila, * Joaquin Ruiz, * Francisco Gallardo, * Martha Vargas, * Lara Soler ([dagger]), Maria Jose Figueras, ([dagger]) and Joaquin Gascon ([double dagger]) * Hospital Clinic, Barcelona, Spain; ([dagger]) Universitat Rovira i Virgili, Reus, Spain; and ([double dagger]) Universitat de Barcelona, Barcelona, Spain Dr. Vila is a professor of microbiology, School of Medicine, University of Barcelona The University of Barcelona (Catalan: Universitat de Barcelona, UB) is a public university located in the city of Barcelona, Catalonia, Spain. It is a member of the Coimbra Group and Joan Lluís Vives Institute. , and consultant to the Clinical Microbiology Laboratory of the Hospital Clinic, Barcelona. His research interests lay in the molecular bases of antimicrobial resistance. |
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