Vol. 25, No. 11JOURNAL OF CLINICAL MICROBIOLOGY, Nov. 1987, p. 2044-20480095-1137/87/112044-05$02.00/0Copyright © 1987, American Society for Microbiology

Clinical Significance of Aeromonas Species Isolated fromPatients with Diarrhea

NELSON P. MOYER

Hygienic Laboratory, University of Iowa, Iowa City, Iowa 52242

Received 11 June 1987/Accepted 3 August 1987

A total of 248 strains ofAeromonas spp. were isolated from 3,334 human fecal specimens submitted to a statepublic health laboratory over a 2-year period to be cultured for enteric pathogens. Cary-Blair transportmedium, blood ampicillin agar, and alkaline peptone water enrichment provided optimal recovery ofAeromonas spp. A questionnaire requesting clinical and epidemiological information was sent to physicians,who submitted stool samples for testing, with each laboratory report for 107 consecutive stool isolates ofAeromonas spp. The 56 questionnaires which were completed and returned were analyzed to determine theseasonal distribution of illness and the age and sex distribution of patients; characteristic symptoms; andpredisposing factors for gastrointestinal disease caused by Aeromonas spp. It was concluded that some A.hydrophila, A. sobria, and A. caviae strains are capable of causing diarrhea and that antibiotic therapy and thedrinking of untreated water are significant risk factors for susceptible hosts.

Aeromonas spp. occur widely in soil and water, wherethey cause diseases in fish and amphibians. They occur inuntreated and chlorinated drinking water, ground beef andpork, fish, shellfish, poultry, produce, and raw milk (4, 6). Avariety of extraintestinal infections have been documentedin humans, and nosocomial infections have been reported inimmunosuppressed patients and patients receiving antibiotictherapy (8, 27).The role of these organisms in gastrointestinal disease is

controversial because of taxonomic and nomenclature va-garies (14, 24) and because of the difficulty in correlatingenterotoxin, cytotoxin, hemolysin, hemagglutinin, and inva-sive properties of clinical isolates with specific symptoms ofdisease (3, 7, 12, 15, 18, 20, 21). A rapidly expanding body ofliterature suggests that Aeromonas spp. cause mild, self-limiting diarrheal disease in previously healthy adults, and aspectrum of intestinal disease ranging from acute dysenteryto chronic watery diarrhea persisting for weeks or monthshas been reported recently (1, 11, 13, 19).Aeromonas spp. cause acute diarrhea in children and

traveler's diarrhea in adults (5, 10). This range of symptomssuggests a complex etiology in which strains possess avariety of virulence factors in different combinations, and atoxigenic mechanism appears most plausible (23). Attemptsto correlate biotype to enteropathogenicity have not beenconsistent, and no pattern of biochemical reactions canpredict whether a particular strain is pathogenic (21). Themost consistent and compelling evidence linking aero-monads to gastrointestinal disease has been epidemiological(10, 16). Holmberg et al. (16) evaluated 34 cases of gastro-enteritis in which Aeromonas spp. were isolated from fecalspecimens, and concluded that some strains of Aeromonascaused diarrhea in previously normal hosts and that organ-isms were probably acquired by the drinking of untreatedwater. The present study was undertaken to characterize thefrequency of isolation and clinical significance ofAeromonasspp. recovered from human fecal specimens submitted to apublic health laboratory by physicians for diagnosis ofdiarrheal disease.

MATERIALS AND METHODS

Culture methods. Unselected fecal specimens (n = 3,334)from patients with diarrhea were submitted in Cary-Blairtransport medium to be cultured for Salmonella, Shigella,Campylobacter, Yersinia, and Aeromonas spp. Primary iso-lation media included MacConkey agar (MCA), xyloselysine desoxycholate agar (XLD), Hektoen agar (HEA),yersinia selective agar (YSA), campy blood agar (CBA),inositol brilliant green agar (IBG), MacConkey Tween agar(MTA), and blood ampicillin agar (BAA). MCA, XLD,HEA, YSA, and CBA were prepared from commercial bases(GIBCO Laboratories, Grand Island, N.Y., or Difco Labo-ratories, Detroit, Mich.) according to the instructions of themanufacturers. IBG was prepared as described by Schubert(25), BAA was prepared as described by Gracey et al. (13),and MTA was prepared as described by Hoban et al. (D.Hoban, T. W. Williams, D. Phippen, and T. J. Louie, Abstr.Annu. Meet. Am. Soc. Microbiol. 1983, C151, p. 336).Specimens were inoculated onto primary plating media witha swab, and the inoculum was cross-streaked with a wireloop. Specimens were also inoculated into gram-negativebroth (GNB), selenite broth (SB), cold enrichment broth(CEB), and 1% alkaline peptone water (APW; pH 8.4) byusing a swab. Both GNB and SB were prepared fromcommercial bases, and CEB was prepared as described byChristenson and Jansen (E. H. Christenson and G. P.Jansen, Abstr. Annu. Meet. Am. Soc. Microbiol. 1977, C43,p. 42). MCA, XLD, and HEA plates were incubated aero-bically at 35°C for 18 to 24 h. YSA plates were incubatedaerobically at 28°C for 24 h. IBG, MTA, and BAA plateswere incubated aerobically at 28°C for 48 h. CBA plates wereinoculated at 42°C in a microaerophilic atmosphere for 48 h.GNB and SB were incubated aerobically for 18 to 24 h at35°C. APW was incubated aerobically for 48 h at ambientlaboratory temperature. CEB was incubated aerobically at4°C for 7 and 14 days. AIl GNB cultures were restreakedonto MCA and XLD plates, while SB cultures wererestreaked onto XLD and HEA plates; and all these plateswere incubated as described above. CEB was restreakedonto YSA plates, which were incubated at 28°C for 24 h.

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TABLE 1. Enteric isolates recovered from 3,334 fecal specimensthat were cultured

No. of isolates in fiscal yr:Organism

1985 1986

Salmonella spp. 56 19Shigella spp. 12 6Campylobacter spp. 31 31Yersinia spp. 6 20Aeromonas spp. 103 145Plesiomonas spp. 1 1

APW was restreaked onto BAA and IBG or MTA, andincubated as described above. Plates were examined forgrowth, and selected colonies were picked for presumptiveidentification by using triple sugar iron agar and lysine ironagar. Campylobacter-like colonies on CBA were screenedfor motility and oxidase production, while colonies from anyplate resembling Aeromonas spp. were screened for theproduction of oxidase. Definitive identification was per-

formed by using conventional biochemical and serologicalmethods.

Questionnaire. The questionnaire designed for this studyasked physicians to record patient identification, address,age, sex, date of onset of illness, diagnosis, presence ofunderlying disease, and duration of illness. Provision wasmade for recording previous medication and whether or notthe diarrheal illness being reported was treated and withwhat medication. A checklist inquired about symptoms,including the presence of diarrhea, number of stools per day,consistency of stools, presence of blood or mucous, occur-rence of abdominal pain or cramping, presence of nausea orvomiting, and fover. Epidemiological questions exploredexposure to fish, frogs, turtles, shellfish, fishing, or swim-ming. Respondents were asked to specify the use of anuntreated private or treated public drinking water supply. Acover letter accompanied each questionnaire explaining thepurpose of the study and provided a summary of clinicalsignificance of Aeromonas spp. present in stool samples.Questionnaires were sent to physicians with each laboratoryreport of an Aeromonas spp. isolated from a stool. Re-sponses from 56 of 107 (52%) questionnaires sent to physi-cians during calendar year 1985 were tabulated to determinethe seasonal distribution of illness and the age and sexdistribution of patients with gastrointestinal disease, charac-teristic symptoms, and possible exposures and predisposingfactors necessary to establish infection.

RESULTS

A total of 3,334 fecal specimens in Cary-Blair transportmedium were cultured for bacterial enteric pathogens duringthe 2-year period from July 1984 through June 1986. Aero-monas spp. were isolated from 238 specimens representing214 patients with diarrheal illness. A total of 248 strains ofAeromonas spp. were isolated because stool samples from10 patients contained two Aeromonas species. The numberofAeromonas isolates, together with isolates of other entericpathogens recovered during the study, are shown in Table 1.Aeromonas spp. were the most frequently isolated orga-nisms during this period.The Aeromonas species that were recovered included A.

caviae (n = 206), A. hydrophila (n = 25), and A. sobria (n =

17). Mixed infections occurred in 24 patients (11%), andother bacterial pathogens that were found concurrently with

Aeromonas spp. included Campylobacter, Shigella, Salmo-nella, Yersinia, and Plesiomonas spp. Giardia lamblia andEntamoeba histolytica were present with Aeromonas spp. insome patients. The bacterial pathogens (isolation rates) wereAeromonas (7.4%), Salmonella (2.2%), Campylobacter(1.9%), Yersinia (0.8%), Shigella (0.5%), and Plesiomonas(0.06%) spp.

Information from questionnaires completed by physiciansfor 56 patients with diarrhea or gastrointestinal complaintsand from which Aeromonas spp. were isolated from fécalspecimens was tabulated and analyzed to characterize thesignificance of Aeromonas spp. as agents of disease. Threecases of giardiasis and one case of salmonellosis wereexcluded from these tabulations. A summary of symptomscaused by Aeromonas spp. is given in Table 2.Recovery of A. caviae was accompanied by diarrhea in

77% (30 of 39) of the reported cases. The frequency ofdiarrhea ranged from 1 to 20 stools per day, with an averagefrequency of 6 stools per day. Abdominal cramps werereported in 69% (27 of 39) of patients from whom a historywas available. Diarrhea was characterized as watery in 56%(22 of 39) and as containing mucus in 23% (9 of 39) of thepatients that were reviewed. Patients with bloody diarrheaincluded two infants (ages, 2 and 3 months), one 20-month-old male, and one 60-year-old male with ulcerative proctitis.A. caviae was the only potential pathogen isolated fromthree of these four patients. The 20-month-old male hadconcurrent infection with A. caviae and A. sobria. Nauseawas reported by 31% (12 of 39) and vomiting by 21% (8 of 39)of patients with available clinical history. The duration ofillness ranged from 3 days to 6 months, with an average of 6weeks. Since fever is not usually associated with diarrhealillness caused by Aeromonas spp., 11 febrile patients wereexamined for other illnesses, and it was discovered that 6patients had received penicillin for otitis media prior to theonset of diarrhea and that 5 of these 6 patients were c2 yearsof age. One patient was treated for a urinary tract infectionprior to developing diarrheal illness. A. caviae was the onlypotential pathogen isolated from the stool samples fromthese 11 patients. A. caviae was recovered from fecalspecimens of nine asymptomatic patients.A. hydrophila infection was characterized by diarrhea in 7

of 9 patients and ranged in frequency from three to ninestools per day, with an average of four stools per day.Abdominal cramps were reported in 7 of 9 patients. Diarrhea

TABLE 2. Symptoms of gastroenteritis caused byAeromonas spp.

No. of patients infected with thefollowing organismsaSymptom

A. caviae A. hydrophila A. sobria(n = 39) (n = 9) (n = 4)

Diarrhea 30 7 3Watery 22 4 3Bloody 4 0 1Mucous 9 0 1Frequency (avg) 1-20/day 3-9/day 5-10/day

(6/day) (4/day) (7/day)Duration (avg) 3 days-6 mo 7 days-1 mo 7 days-3 wk

(6 wk) (3 wk) (1 wk)Cramps 27 7 2Nausea 12 3 3Vomiting 8 2 2Fever il0 0

an indicates number of patients.

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TABLE 3. Organisms present in mixed infections

LaboratoryPatient Sex' Age Diagnosis findings

A F 20 mo Enteritis A. sobria,A. caviae

B F 28 yr Salmonellosis A. hydrophilia,Salmonellaanatum

C M 2 mo Diarrhea A. hydrophila,A. caviae

D M 21 yr Not given A. hydrophila,A. caviae

E M 49 yr Diarrhea A. hydrophila,A. caviae

F F 70 yr Enteritis A. hydrophila,A. caviae

G F 25 yr Diarrhea A. hydrophila,A. cavine

H M 2 yr Giardiasis A. caviae,G. lamblia

I F 33 yr Giardiasis A. caviae,G. lamblia

J F 47 yr Giardiasis A. caviae,G. lamblia

K F 21 yr Amebiasis A. caviae,E. histolvtica

L M 7 yr Abdominal A. caviae,pain B. hominis

M F 20 yr Gastroenteritis A. caviae,yeasts

a F. Female; M, male.

was characterized as watery (4 of 9 patients), but no blood ormucus was reported. Nausea (3 of 9 patients) and vomiting (2of 9 patients) were not prominent symptoms, and no feverwas reported. The duration of illness ranged from 7 to 30days, with an average of 20 days. One patient had experi-enced diarrhea for 3 years.

A. sobria infection was characterized by diarrhea in threeof four patients from whom a history was available. Threestool samples were watery, one was bloody, and one con-tained mucus. The frequency of diarrhea was 5 to 10 stoolsper day, with an average of 7 stools per day. Nausea (threeof four patients), cramps (two of four patients), and vomiting(two of four patients) were reported, but no fever occurred.The duration of illness ranged from 1 to 3 weeks, with an

average of 1 week.Physicians were asked to record a clinical diagnosis for the

illness of the patient. Diarrhea, gastroenteritis, and dysen-tery were reported in 84% (41 of 49) of patients from whichAeromonas spp. were isolated in the absence of otherintestinal pathogens. Other diagnoses included ulcerativeproctitis (n = 1), amebiasis (n = 1), giardiasis (n = 3),salmonellosis (n = 1), and diarrhea attributed to Blastocystishominis (n = 1) and yeasts (n = 1). The nonspecific diag-noses that were mentioned included abdominal pain (n = 2),spastic colon (n = 2), cachexia (n = 1), irritable bowelsyndrome (n = 1), and malaise and depression (n = 1); andAeromonas spp. were the only potential pathogenic orga-nisms isolated from these patients.Concurrent infection with more than one enteric pathogen

occurred in 24 patients during the 2-year period of the study,and histories were available for 13 patients. Data on age,

sex, diagnosis, and laboratory findings for these cases are

presented in Table 3. A. caviae was isolated in 12 of 13mixed infections. Aeromonas spp. were the only entericpathogens isolated in 6 of 13 cases.

The seasonal distribution of all enteric pathogens thatwere isolated is shown in Fig. 1. Peak incidence for recoveryof Aeromonas spp. occurred in summer and fall months;however, cases occurred throughout the year.

Analysis of 56 patients by sex revealed 22 cases of illnessin males and 34 cases in females. A. hydrophila infectionoccurred slightly more frequently in adult males (6 of 9),while A. sobria exhibited equal sex distribution. A. caviaewas recovered more frequently from adult females (20 of 27),who experienced twice the infection rate of men. A. caviaeinfection (9 of 13) was more common among male children-3 years of age. Age and sex distributions of patients isshown in Fig. 2. Diarrhea occurred in all age groups, but itoccurred more frequently in children under the age of 3 years(30%) and in middle-age adults (30%).

Physicians were asked to indicate prediagnosing factorswhich could allow colonization of the intestinal tract by anopportunistic pathogen. A list of antimicrobial agents pre-scribed prior to the onset of diarrhea included penicillin (n =1), ampicillin (n = 5), and cephalexin (n = 1). A. caviae wasisolated from each of these patients. Trimethoprim-sulfamethoxazole was used to successfully treat the diar-rheal illness in nine patients with infections caused by A.caviae, and doxycycline was used to successfully treat onepatient with diarrhea caused by A. hydrophila.When physicians were questioned about the source of

infection, associations identified included ingestion of shell-fish (n = 3), fishing (n = 4), and swimming in untreatedsurface water (n = 4). One patient with gastroenteritiscaused by A. hydrophila was employed in a fish market.Patients were asked if they regularly consumed water fromtreated or untreated supplies. The drinking of untreatedwater was reported by 54% (26 of 48) respondents, includingpatients who were culture positive for A. sobria (n = 1), A.hydrophila (n = 6), and A. caviae (n = 19). Of 22 patientsthat drank treated water, cultures yielded A. sobria (n = 3),A. hydrophila (n = 1), and A. caviae (n = 18). No statisticalassociation was shown between consumption of water frompublic or private sources; however, exposure to water wasthe most likely source of Aeromonas spp. for 86% (46 of 56)of the cases reported. There was no evidence of familialfecal-oral transmission from this study.

DISCUSSION

The culture methods for transport, enrichment, and recov-ery of Aeromonas spp. proved sensitive since they wererecovered with greater frequency than all other entericpathogens. Cary-Blair transport medium allowed the recov-ery of Aeromonas spp. that were in transit from 1 to 8 daysbetween collection and culture in the laboratory. Optimalrecovery of aeromonads occurred when BAA was used withAPW enrichment. Results of studies of ampicillin suscepti-bility in Aeromonas spp. indicate that most strains areresistant to a concentration of 10 ,ug/ml (22), whereas higherconcentrations recommended by some investigators may beinhibitory to a significant percentage of strains (26). Sincecompletion of this study, the use of MTA and IBG wasdiscontinued because it was nonproductive, despite pub-lished recommendations (2, 26).

Results of studies in the United States and abroad haveshown asymptomatic carriage rates from 0.1 to 27%, de-pending on the population screened and the culture methodsemployed (1, 13). The use of enrichment and selective mediafor the isolation ofAeromonas spp. from fecal specimens hasbeen criticized as being too sensitive by some investigators

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20

! YersiniaO Shigella| CampylobacterEJ SalmonellaEl Aeromonas

Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun

FY85 FY86

FIG. 1. Monthly distribution of enteric pathogens isolated during fiscal years (FY) 1985 and 1986.

or too insensitive by others because of inhibitionAeromonas which are sensitive to selective agen

media or ampicillin (9, 15, 16). ApproximatelyAeromonas spp. isolated in this study grew on bcand nonselective media, and 75% of al Aerorrtions occurred on primary plating media before tThe problems of inhibitory overgrowth by normeon nonselective media; the logistics of examinintypes appearing on enteric culture media for oxidtion; and the recognized problem of false-negatreactions on media containing carbohydrates, bildyes make the use of nonselective and comic

enteric culture media impractical for the isolatimonas spp. from fecal specimens (17).

Results of this study suggest that Aeromonasgastroenteritis, ranging from acute illness inchronic illness in adults. Diarrhea (40 of 52 pEabdominal cramps (36 of 52 patients) were the psymptoms with all three Aeromonas spp. Gawcaused by A. sobria and A. hydrophila tended twhile diarrhea associated with A. caviae was

chronic, with a duration of 4 to 6 weeks irpatients.Although A. caviae has been considered non

five pediatric patients with otitis media who W'with penicillin or ampicillin subsequently developin which A. caviae was the sole potential enteri

25

20

15

cc

o 10-

z * 7777r71s

0-5 6-9 10-19 20-29 30-39 40-49 50-59 60-69

Age (Years)

FIG. 2. Distribution of cases of enteritis caused bspp. by age and sex.

of strains of Four of these children obtained water from an untreatedts in enteric private source, and the source for one child was not avail-50% of the able. Antibiotic therapy with drugs to which Aeromonasth selective spp. are resistant probably contributed to colonization of theionas isola- gastrointestinal tract of these patients with A. caviae, withenrichment. the subsequent development of acute diarrhea. These fourAi fecal flora patients (ages 2 or under) were treated with trimethoprim-ig all colony sulfamethoxazole, and their symptoms were resolved. Nolase produc- treatment record was available for one 14-year-old patient.ive oxidase Additional evidence to support the role of A. caviae as an

le salts, and enteric pathogen was the occurrence of bloody diarrhea inonly used three children under the age of 2 years in the absence ofon of Aero- other potential bacterial pathogens.

Drinking or swimming in untreated water was the mostspp. cause frequently identified exposure in cases in which A. caviaeinfants to was cultured from fecal specimens. The source of A.

patients) and hydrophila infections was identified as shellfish (2 of 9redominant patients), fishing (2 of 9 patients), and the drinking ofstroenteritis untreated water (6 of 9 patients). No exposure was reportedto be acute, for the four patients with A. sobria.frequently In those cases in which patient age was given, A.

n untreated hydrophila infections occurred most frequently in adultmales (6 of 9 patients), while A. caviae was recovered most

pathogenic, frequently from the stools of adult females (20 of 27 pa-vere treated tients). No explanation is apparent.?ed diarrhea Most investigators accept A. hydrophila and A. sobria as

c pathogen. being enteric pathogens that are capable of causing gastro-enteritis, in addition to a variety of extraintestinal infections.Enterotoxins, cytotoxins, and hemolysins have been studiedto elucidate a mechanism by which Aeromonas spp. producediarrhea; but no convincing causal relationships have been

* Maie established. Epidemiological evidence for the pathogenicity2 Female of opportunistic Aeromonas spp. has been presented by

Holmberg et al. (16). They found a clear association betweenthe drinking of untreated water and the occurrence ofchronic gastroenteritis in adults and acute gastroenteritis inchildren. They presented evidence that A. caviae may causediarrhea and isolated identical biotypes from a patient and

E////X her children and from another patient and her well water. We

have extended this study by obtaining additional epidemio-70-79 8089 logical information to support a causal role for some strains

of A. caviae as an opportunistic cause for gastroenteritis. A.y Aerormonas caviae colonies the intestinal tract, producing acute diar-

rhea following antibiotic treatment, and causes chronic

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diarrhea in susceptible adults with long-term exposure tosources of organisms.

ACKNOWLEDGMENTS

I thank Patricia J. Quinn, Carol A. Showalter, Larry A. Holcomb,Paul A. Holton, and James P. Nelson for technical support. CarilynM. Wieland and staff typed the manuscript and Theodore W. Healdprovided graphic assistance.

LITERATURÉ CITED

1. Agger, W. A., J. D. McCormick, and M. J. Gurwith. 1985.Clinical and microbiological features of Aeromonas hydrophila-associated diarrhea. J. Clin. Microbiol. 21:909-913.

2. Altorfer, R., M. Altwegg, J. Zollinger-Iten, and A. vonGraevenitz. 1985. Growth of Aeromonas spp. on cefsulodin-iragasan-novobiosin agar selective for Yersinia enterocolitica. J.Clin. Microbiol. 22:478-480.

3. Atkinson, M., Il., and T. J. Trust. 1980. Hemagglutinationproperties and adherence ability of Aeromonas hydrophila.Infect. Immun. 27:938-946.

4. Buchanan, R. L., and S. -A. Palumbo. 1985. Aeromonashydrophila and Aeromonas sobria as potential food poisoningspecies: a review. J. Food Safety 7:15-29.

5. Burke, V., M. Gracey, J. Robinson, D. Peck, J. Beaman, and C.Bunidell. 1983. The microbiology of childhood gastroenteritis:Aeromonas species and other infective agents. J. Infect. Dis.148:68-74.

6. Burke, V., J. Robinson, M. Gracey, D. Peterson, and K. Par-tridge. 1984. Isolation of Aeromonas hydrophila from a metro-politan water supply: seasonal correlation with clinical isolates.Apple. Environ. Microbiol. 48:361-366.

7. Chopra, A. K., C. W. Houston, C. T. Genaux, J. D. Dixon, andA. Kurosky. 1986. Evidence for production of an enterotoxinand cholera toxin cross-reactive factor by Aeromonas hydro-phila. J. Clin. Microbiol. 24:661-664.

8. Daily, O. P., S. W. Joseph, J. C. Coolbaugh, R. I. Walker, B. R.Merrell, Di M. Rollins, R. H. Seidler, R. R. Colwell, and C. R.Lissner. 1981. Association of Aeromonas with human infection.J. Clin. Microbiol. 13:769-777.

9. Desmond, E., and J. M. Jànda. 1986. Growth of Aeromonasspecies on enteric agars. J. Clin. Microbiol. 23:1065-1067.

10. Echeverria, P., N. R. Blacklow, L. B. Sanford, and G. C. Cukor.1981. Traveler's diarrhea among American Peace Corps volun-teers in rural Thailand. J. Infect. Dis. 143:767-771.

11. George, W. L., M. M. Nakata, J. Thompson, and M. L. White.1985. Aeromonas-related diarrhea in adults. Arch. Intern. Med.145:2207-2211.

12. Goodwin, C. S., W. E. S. Harper, J. K. Steward, M. Gracey, V.Burke, and J. Robinson. 1983. Enterotoxigenic Aeromonashydrophila and diarrhoea in adults. Med. J. Aust. 1:25-26.

13. Gracey, M., V. Burke, and J. Robinson. 1982. Aeromonas-associated gastroenteritis. Lancet i:1304-1306.

14. Hickman-Brenner, F. W., K. L. MacDonald, A. G. Steigerwalt,G. R. Fanning, D. J. Brenner, and J. J. Farmer, III. 1987.Aeromonas veronii, a new ornithine decarboxylase-positivespecies that may cause diarrhea. J. Clin. Microbiol. 25.900-906.

15. Holmnberg, S. D., and J. J. Farmer III. 1984. Aeromonashydrophila and Plesiomonas shigelloides as causes of intestinalinfections. Rev. Infect. Dis. 6:633-639.

16. Holmberg, S. D., W. L. Schell, G. R. Fanning, L. K. Wachsmith,F. W. Hickman-Brenlner, P. A. Blake, D. J. Brenner, and J. J.Farmer III. 1986. Aeromonas intestinal infections in the UnitedStates. Ann. Intern. Med. 105:683-689.

17. Kay, B. A., C. E. Guerrero, and R. B. Sack. 1985. Media for theisolation of Aeromonas hydrophila. J. Clin. Microbiol. 22:888-890.

18. Kindschuh, M., L. K. Pickering, T. G. Cleary, and G. Ruiz-Palacios. 1987. Clinical and biochemical significance of toxinproduction by Aeromonas hydrophila. J. Clin. Microbiol. 25:916-921.

19. Kipperman, H., M. Ephros, M. Lambdin, and K. White-Rogers.1984. Aeromonas hydrophila: a treatable cause of diarrhea.Pediatrics 73:253-254.

20. Kirov, S. M., B. Rees, R. C. Wellock, J. M. Goldsmid, and A. D.Van Galen. 1986. Virulence characteristics of Aeromonas spp.in relation to source and biotype. J. Clin. Microbiol. 24:827-834.

21. Morgan, D. R., P. C. Johnson, H. L. DuPont, T. K. Satterwhite,and L. V. Wood. 1985. Lack of correlation between knownvirulence properties ofAeromonas hydrophila and enteropatho-genicity for humans. Infect. Immun. 50:62-65.

22. Motyl, M. R., G. McKinley, and J. M. Janda. 1985. In vitrosusceptibilities of Aeromonas hydrophila, Aeromonas sobria,and Aeromonas caviae to 22 antimicrobial agents. Antimicrob.Agents Chenmother. 28:151-153.

23. Notermans, S., A. Havelaar, W. Jansen, S. Kozaki, and P.Guinee. 1986. Production of "Asao toxin" by Aeromonasstrains isolated from feces and drinking water. J. Clin. Micro-biol. 23:1140-1142.

24. Popoff, M., C. Coynault, M. Kiredjian, and M. Lemelin. 1981.Polynucleotide sequence relatedness among motile Aeromonasspecies. Curr. Microbiol. 5:109-114.

25. Schubert, R. H. W. 1977. Uber den Nachweis von Plesiomonasshigelloides lIabs and Schubert, 1962, and ein elektive Mediumden inositol brillantgrun gallesalz Agar. E. Rodenwalat-Archiv.4:97-103.

26. Von Graevenitz, A., and C. Bucher. 1983. Evaluation of differ-ential and selective media for isolation of Aeromonas andPlesiomonas spp. from human feces. J. Clin. Microbiol. 17:16-21.

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