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Clinical features of Aeromonas enteritis in Hawaii
126
SOCIETY OFTROPICALMEDICINE ANDHYGIENE (1990) 84, 126-128 TRANSACTIONSOF THE ROYAL
Clinical features
of Aeromonas
enteritis
in Hawaii
Daniel L. Phillips, Francis D. Pien and Thomas A. Leong Struub Clinic and Hospital, Inc., University of A. Burns School of Medici’ne, Honolulu, Hawaii
Hawaii-John
Abstract The incidence and clinical features of enteritis associatedwith Aeromonas in Honolulu were studied. The stool isolation rate was 2.9% for Aeromomzs. the third most common bacterial pathogen in this population. Clinical features of Aeromonas-associatedenteritis were compared with clinical features of enteritis without an associated bacterial pathogen. Although there was a trend toward more abdominal pain, tenderness, nausea and prolonged illness in patients with Aer omo~s, these differences were not statistically significant. In most cases,Aeromonas enteritis is a self-limited illness, indistmguishable from other causes of diarrhoea seen in our clinic. Introduction
Aeromonas are Gram-negative, oxidase-positive bacteria, which include non-motile A. salmonicidu and a second group of motile bacteria consisting of at least 3 species: A. hydrophila, A. caviae, and A. sobriu (POPOFF,1984). Strong epidemiolomcal evidence has suggested that some Aeromonus strains produce gastrointestinal illness (BURKE et al., 1983a; ECHEVERRIA et al., 1981; HOLMBERGet al., 1986); most intriguing have been reports that some Aeromonus produce dysenteric illness (AGGERet al., 1985; GRACEY et al., 1982; HOLMBERCet al., 1986; WATSON et al., 1985). However, other evidence disputes the gastrointestinal role of Aer omonm. A. caviae, which usually does not produce enterotoxin (BURKE et al., 1983b), is the most common species isolated in Aeromonas-associated diarrhoea in the United States (MOYER, 1987; TRAVIS81WASHINGTON,1986). Furthermore, ingestion studies with different Aeromonas strains have failed to produce diarrhoea in human volunteers (MORGANet al., 1985). Therefore, some investigators have suggested that Aeromonus may be a colonizer in patients rather than a causative agent of diarrhoea (FIGURAet al., 1986; TRAVIS & WASHINGTON, 1986). We previously studied Campylobacter jejuni enteritis in Honolulu and compared clinical features of this illness with those of patients with diarrhoea from whom no bacterial pathogen was isolated (PIEN et al., 1983). In that study, Campylobacter enteritis was associated with a significantly higher incidence of abdominal pain, fever, bloody stool and faecal leucocytes. A 1987 pilot study of 15 of our clinic Datients with Aeromona&associateh enteritis suggesteh prolonged diarrhoeal illness with a hieh incidence of haematochezia (unpublished data).“We therefore undertook a large investigation to define the incidence of Aeromonas enteritis in our clinic and compare clinical features of Aeromona s-associated diarrhoeal illness with enteritis in which no bacterial pathogen was isolated. In addition, we studied whether Aeromonas enteritis was associated with prolonged symptoms
when compared to a control group of patients with diarrhoea due to other causes.We speculated that the previously reported prolonged diration of illness (mean: 42 d in adults and 19 d in children) in patients with Aer omonus(HOLMBERGet al., 1986)hay have been a consequence of patient selection; their study population included only patients from whom physicians obtained stool cultures, without a control group with negative stool cultures. Finally, we examined a subgroup of patients infected with Aeromauls strains thought most likely to produce enterotoxin. A previous report suggested that Aeromonas strait which give positive reaction in the VogesProskauer (VP) and lysine decarboxylase (LDC) tests and do not ferment arabinose were more likely to produce enterotoxin (BURKE et al., 1983b). We compared patients with Aeromonus that were VP positive, LDC positive and arabinose negative, to patients with other Ae~omonus sp. Materials and Methods Straub Clinic is a group practice of 130 physicians located on Oahu and serves a patient population of 120 000. From 1 January 1987 to 30 June 1988, 1561 consecutive stool specimens were cultured on sheep blood agar, McConkey agar, Hektoen agar and G. N. broth (EWING, 1986). Suspected Aeromona s isolates were tested for oxidase activity. Oxidase positive, beta-haemolytic, Gram-negative bacteria were innoculated in API 20E strips (Analytab, Plainview, New York) for Aeromonus identification. Testing for enterotoxin production was not done. The immediately preceding and following patients who had negative bacterial stool cultures were selected as a control population. Medical records from both Aeromonas and control patients were retrospectively reviewed for enidemioloeical and clinical features. When natients &d not ret& for follow-up, it was assumedX for the purpose of this study that their illness stopped at their last physician contact. Statistical analysis was performed using &i-square for categorical data, t test for continuous data, and a non-parametric median test for non-normal continuous data. Results Forty-four stool cultures with Aer omonus were identified. In 2 cases, there was insufficient clinical Table 1. Bacterial pathogens isolated at Straub Clinic, January 1987-30 June 1988
Bacteria Aeromonas sp. Campylobacterjejuni Salmonella sp. Shigella sp. No oathoeen
No. of patient isolates
44
100 55 13:;
Percentof total
stool specimens 2.9 6.4 3.5 8:.:
1
127 Table
2. Clinical
features
of Aeromonas
enteritis
Percentage ofA;ESwith No bacterial pathogen
Clinical characteristics Outpatient Female sex Prior antibiotics Gastrointestinal associated disease Immunosuppression History of fever Abdominal pain Nausea Haematochezia Elevated temperature
27 (84)
:i g;
O-630 0.266 0.563 0.107 O-316 0.916 0.129 0.114 o-100
:i g; 42 (48)
:i [::j 40 (25)
0.695 o-052 O-986
it [ii;”
!Z [it{
2z $8 13 (84)
2: g:; 7 (42)
ii i:z; 44 (54)
is g{
(>375”C)
Abdominal tenderness Occult blood in stool
P
“Probability of difference occurring by chance (x2 test). bNumbers in parentheses are numbers of patients studied.
30
0
25
Patients with no pathogen Patients with Aeromonas
O-4
5-9
lo-14 15-19 20-24 25-29 30-34 35-39 40-44 45-49 50-54 55-59 SO
Duration
of illness (days)
Figure. Duration of illness in patients with and without Aeromotzas infection. information to perform meaningful analysis; these cases were excluded together with 4 companion control patients. Table 1 demonstrates the frequency of bacterial pathogens isolated in our laboratory. Aeromows was the third most common bacterial enteric pathogen (2.9% of stool culture specimens). There was no seasonalpattern of Aeromona s isolation. The mean ages of patients with Aetomonas
(38.62k23.05 years) and patients without pathogens (38.19+26*16 years) were not significantly different (P=O*930). Table 2 compares clinical E;gzi E patients with and without Aeromotua . parentheses represent the total number of patients from whom complete clinical information was available. There were no statistically significant differences between the 2 groups (P
128 gastrointestinal diseaseand haematocheziawere more common in the control group and nausea, abdominal pain and abdominal tenderness were more frequent in patients with Aeromonas. The figure shows durations of illness for both patient groups. Patients with Aeromma s had a longer median duration of illness (135 vs 10 d), but this difference was not significant (by the median test). When patients with diarrhoea lasting either more than 90 d or less than one day were omitted, the trend toward longer duration of illness for patients with Aerommzs was more evident (median values for durations of illness were 9.5 d and 14.0 d for pathogen-free and Aeromona s patients, respectively); however, this difference still did not attain statistical significance (median test, O*O%P
This study demonstrated no significant differences between patients with stool cultures with Aetvmonas and patients with bacteriologically negative stool cultures. Furthermore, we found that the use of VP, LDC and arabinose reactions to identify putative enterotoxin-producing Aeromonas strains was not helpful in distinguishing a subgroup that produced more severe diarrhoeal illness. We also found that was not statistidiarrhoea associatedwith Aerms cally different in duration from diarrhoea in control patients, although there was a trend towards longers. There lasting symptoms in patients with Aerare several possible explanations for our findings. Aermtmas may not be a pathogen but merely a colonizer in patients with diarrhoea. Alternatively, Aerumonus may produce diarrhoeal illness which is indistinguishable from that found in other patients with diarrhoea. Lastly, perhaps there were too few patients with Aeromona s to produce statistically significant differences in our study (type II error). There are weaknessesin our study becauseof its retrospective nature. Clinical information was abstracted from records which were not always complete. Secondly, duration of illness data were limited because patients did not alwavs return for follow-un visits. This would tend to bias-the duration of the ;llness to a shorter period of time than actually occurred. However, this bias should have applied equally to the control group. In conclusion, we think that the majority of patients from whom stool cultures are positive for Aerommus will have illness indistinauishable from other causes of diarrhoea seen in ou; clinic, and in most casesthis illness is self-limited. Although trends towards prolonged duration with increased abdominal pain, nausea, and tenderness occurred in Aeromms patients, statistical significance was not shown. The question arises whether patients who have stool s should receive antibiocultures positive for Aerw tic therapy. Although our study was not designed to answer this question, antibiotic therapy may not be
necessaryfor most patients with Aerommu s. Whether the subset of patients who have a more prolonged illness will benefit from antibiotic therapy warrants further investigation. AcknowledPements We thar& Ann Harada for statistical assistance, Emily Chun for transcriptional assistance, and Dr Howard Minami for advice with project design. The project was funded by The Straub Medical Research and Education Foundation. Mr Leong was supported by the Pacific Health Research Institute Summer Scholarship Program. References Aggar, W. A., McCormick, J. D. & Gut-with, M. J. (1985). Clinical and microbiolonical features of Aeronwnus hvdmph&z-associated diarrhoea. Journal of Clinical M&obiolom. 21. 909-913. Burke, V., Gracey, M.,-Robinson, J., Peck, D., Beaman, J. & Btmdell, C. (1983a). The microbiology of childhood gastroenteritis: ~Aero&nus species and-other infective agents. Journal of Infectious Diseases, 148, 68-74. Burke, V., Robinson, J., Beaman, J., Gracey, M., Lesmana, M., Rockhill, R., Echeverria, P. & Janda, J. M. (1983b). Correlation of enterotoxicity with biotype in Aeromonas spp. Journal of Clinical Microbiology, 18, 119~1200. Echeverria, P., Blacklow, N. R., Sanford, L. B. & Cukor, G. G. (1981). Travelers’ diarrhea among American Peace Corp volunteers in rural Thailand. 3oumal of Infectious Diseases, 143, 767-771. Ewing, W. H. (1986). Edwards and Ewing’s Ident$ication of Enterobactmiaceae, 4th edition. New York: Elsevier Science Publishing Company, pp. 2745. Figura, N., Marri, L., Verdiani, S., Ceccherini, C. & Barben, A. (1986). Prevalence, species differentiation, and toxigenicity of Aeromonas strains in cases of childhood gastroenteritis and in controls. 3ournul of Clinical Microbiology, 23, 595-599. Gracey, M., Burke, V. & Robinson, J. (1982). Aerommasassociated gastroenteritis. Lancet, ii, 1304-1306. Holmberg, S. D., Schell, W. L., Fanning, G. R., Wachsmuth, I. K., Hickman-Brenner, F. W., Blake, P. A., Brenner, D. J. & Farmer, J. J. III (1986). Aeromonas intestinal infections in the United States. Annals of Internal Medicine, 105, 683-689. Morgan, D. R., Johnson, P. C., Cad&l, P., DuPont, H. L., Satterwhite, T. K. & Wood, L. V. (1985). Lack of correlation between known virulence properties of Aeromoms hydrophila and enteropathogenicity for humans. Infection and Immuniry, 50, 62-65. Moyer, N. P. (1987). Clinical significance of Aeronwnas species isolated from patients with diarrhea. 3ournal of Clinical Microbiology, 25, 2044-2048. Pien, F. D., Hsu, A. K., Padua, S. A., Isaacson, N. S. & Naka, S. (1983). Campylobacter jejuni enteritis in Honolulu, Hawaii. Transactions of the Royal Society of Troptcal Medicine and Hygiene, 77, 492-494. Pouoff. M. (1984). Aemmmm. In Bureev’s Manual of ~S$matic‘Bact&ology, vol. l., Krieg, N.< R. & Holt, J. G. (editors). Baltimore: Wilhams and Wilkins, pp. 545-548. Travis, L. B. & Washington, J. A. II (1986). Thisat significance of stool isolates of Amnnona . Journal of Clinical Pathology, 85, 330-336. Watson, I. M., Robinson, J. O., Burke, V. & Gracey, M. (1985). Invasiveness of Aeromonus spp. in relation to biotype, virulence factors, and clinical features. Journ of Clinical Microbiology, 22, 48-51. --I
Received
--I
3 May
August 1989
1989;
accepted
for
publication
15
SOCIETY OFTROPICALMEDICINE ANDHYGIENE (1990) 84, 126-128 TRANSACTIONSOF THE ROYAL
Clinical features
of Aeromonas
enteritis
in Hawaii
Daniel L. Phillips, Francis D. Pien and Thomas A. Leong Struub Clinic and Hospital, Inc., University of A. Burns School of Medici’ne, Honolulu, Hawaii
Hawaii-John
Abstract The incidence and clinical features of enteritis associatedwith Aeromonas in Honolulu were studied. The stool isolation rate was 2.9% for Aeromomzs. the third most common bacterial pathogen in this population. Clinical features of Aeromonas-associatedenteritis were compared with clinical features of enteritis without an associated bacterial pathogen. Although there was a trend toward more abdominal pain, tenderness, nausea and prolonged illness in patients with Aer omo~s, these differences were not statistically significant. In most cases,Aeromonas enteritis is a self-limited illness, indistmguishable from other causes of diarrhoea seen in our clinic. Introduction
Aeromonas are Gram-negative, oxidase-positive bacteria, which include non-motile A. salmonicidu and a second group of motile bacteria consisting of at least 3 species: A. hydrophila, A. caviae, and A. sobriu (POPOFF,1984). Strong epidemiolomcal evidence has suggested that some Aeromonus strains produce gastrointestinal illness (BURKE et al., 1983a; ECHEVERRIA et al., 1981; HOLMBERGet al., 1986); most intriguing have been reports that some Aeromonus produce dysenteric illness (AGGERet al., 1985; GRACEY et al., 1982; HOLMBERCet al., 1986; WATSON et al., 1985). However, other evidence disputes the gastrointestinal role of Aer omonm. A. caviae, which usually does not produce enterotoxin (BURKE et al., 1983b), is the most common species isolated in Aeromonas-associated diarrhoea in the United States (MOYER, 1987; TRAVIS81WASHINGTON,1986). Furthermore, ingestion studies with different Aeromonas strains have failed to produce diarrhoea in human volunteers (MORGANet al., 1985). Therefore, some investigators have suggested that Aeromonus may be a colonizer in patients rather than a causative agent of diarrhoea (FIGURAet al., 1986; TRAVIS & WASHINGTON, 1986). We previously studied Campylobacter jejuni enteritis in Honolulu and compared clinical features of this illness with those of patients with diarrhoea from whom no bacterial pathogen was isolated (PIEN et al., 1983). In that study, Campylobacter enteritis was associated with a significantly higher incidence of abdominal pain, fever, bloody stool and faecal leucocytes. A 1987 pilot study of 15 of our clinic Datients with Aeromona&associateh enteritis suggesteh prolonged diarrhoeal illness with a hieh incidence of haematochezia (unpublished data).“We therefore undertook a large investigation to define the incidence of Aeromonas enteritis in our clinic and compare clinical features of Aeromona s-associated diarrhoeal illness with enteritis in which no bacterial pathogen was isolated. In addition, we studied whether Aeromonas enteritis was associated with prolonged symptoms
when compared to a control group of patients with diarrhoea due to other causes.We speculated that the previously reported prolonged diration of illness (mean: 42 d in adults and 19 d in children) in patients with Aer omonus(HOLMBERGet al., 1986)hay have been a consequence of patient selection; their study population included only patients from whom physicians obtained stool cultures, without a control group with negative stool cultures. Finally, we examined a subgroup of patients infected with Aeromauls strains thought most likely to produce enterotoxin. A previous report suggested that Aeromonas strait which give positive reaction in the VogesProskauer (VP) and lysine decarboxylase (LDC) tests and do not ferment arabinose were more likely to produce enterotoxin (BURKE et al., 1983b). We compared patients with Aeromonus that were VP positive, LDC positive and arabinose negative, to patients with other Ae~omonus sp. Materials and Methods Straub Clinic is a group practice of 130 physicians located on Oahu and serves a patient population of 120 000. From 1 January 1987 to 30 June 1988, 1561 consecutive stool specimens were cultured on sheep blood agar, McConkey agar, Hektoen agar and G. N. broth (EWING, 1986). Suspected Aeromona s isolates were tested for oxidase activity. Oxidase positive, beta-haemolytic, Gram-negative bacteria were innoculated in API 20E strips (Analytab, Plainview, New York) for Aeromonus identification. Testing for enterotoxin production was not done. The immediately preceding and following patients who had negative bacterial stool cultures were selected as a control population. Medical records from both Aeromonas and control patients were retrospectively reviewed for enidemioloeical and clinical features. When natients &d not ret& for follow-up, it was assumedX for the purpose of this study that their illness stopped at their last physician contact. Statistical analysis was performed using &i-square for categorical data, t test for continuous data, and a non-parametric median test for non-normal continuous data. Results Forty-four stool cultures with Aer omonus were identified. In 2 cases, there was insufficient clinical Table 1. Bacterial pathogens isolated at Straub Clinic, January 1987-30 June 1988
Bacteria Aeromonas sp. Campylobacterjejuni Salmonella sp. Shigella sp. No oathoeen
No. of patient isolates
44
100 55 13:;
Percentof total
stool specimens 2.9 6.4 3.5 8:.:
1
127 Table
2. Clinical
features
of Aeromonas
enteritis
Percentage ofA;ESwith No bacterial pathogen
Clinical characteristics Outpatient Female sex Prior antibiotics Gastrointestinal associated disease Immunosuppression History of fever Abdominal pain Nausea Haematochezia Elevated temperature
27 (84)
:i g;
O-630 0.266 0.563 0.107 O-316 0.916 0.129 0.114 o-100
:i g; 42 (48)
:i [::j 40 (25)
0.695 o-052 O-986
it [ii;”
!Z [it{
2z $8 13 (84)
2: g:; 7 (42)
ii i:z; 44 (54)
is g{
(>375”C)
Abdominal tenderness Occult blood in stool
P
“Probability of difference occurring by chance (x2 test). bNumbers in parentheses are numbers of patients studied.
30
0
25
Patients with no pathogen Patients with Aeromonas
O-4
5-9
lo-14 15-19 20-24 25-29 30-34 35-39 40-44 45-49 50-54 55-59 SO
Duration
of illness (days)
Figure. Duration of illness in patients with and without Aeromotzas infection. information to perform meaningful analysis; these cases were excluded together with 4 companion control patients. Table 1 demonstrates the frequency of bacterial pathogens isolated in our laboratory. Aeromows was the third most common bacterial enteric pathogen (2.9% of stool culture specimens). There was no seasonalpattern of Aeromona s isolation. The mean ages of patients with Aetomonas
(38.62k23.05 years) and patients without pathogens (38.19+26*16 years) were not significantly different (P=O*930). Table 2 compares clinical E;gzi E patients with and without Aeromotua . parentheses represent the total number of patients from whom complete clinical information was available. There were no statistically significant differences between the 2 groups (P
128 gastrointestinal diseaseand haematocheziawere more common in the control group and nausea, abdominal pain and abdominal tenderness were more frequent in patients with Aeromonas. The figure shows durations of illness for both patient groups. Patients with Aeromma s had a longer median duration of illness (135 vs 10 d), but this difference was not significant (by the median test). When patients with diarrhoea lasting either more than 90 d or less than one day were omitted, the trend toward longer duration of illness for patients with Aerommzs was more evident (median values for durations of illness were 9.5 d and 14.0 d for pathogen-free and Aeromona s patients, respectively); however, this difference still did not attain statistical significance (median test, O*O%P
This study demonstrated no significant differences between patients with stool cultures with Aetvmonas and patients with bacteriologically negative stool cultures. Furthermore, we found that the use of VP, LDC and arabinose reactions to identify putative enterotoxin-producing Aeromonas strains was not helpful in distinguishing a subgroup that produced more severe diarrhoeal illness. We also found that was not statistidiarrhoea associatedwith Aerms cally different in duration from diarrhoea in control patients, although there was a trend towards longers. There lasting symptoms in patients with Aerare several possible explanations for our findings. Aermtmas may not be a pathogen but merely a colonizer in patients with diarrhoea. Alternatively, Aerumonus may produce diarrhoeal illness which is indistinguishable from that found in other patients with diarrhoea. Lastly, perhaps there were too few patients with Aeromona s to produce statistically significant differences in our study (type II error). There are weaknessesin our study becauseof its retrospective nature. Clinical information was abstracted from records which were not always complete. Secondly, duration of illness data were limited because patients did not alwavs return for follow-un visits. This would tend to bias-the duration of the ;llness to a shorter period of time than actually occurred. However, this bias should have applied equally to the control group. In conclusion, we think that the majority of patients from whom stool cultures are positive for Aerommus will have illness indistinauishable from other causes of diarrhoea seen in ou; clinic, and in most casesthis illness is self-limited. Although trends towards prolonged duration with increased abdominal pain, nausea, and tenderness occurred in Aeromms patients, statistical significance was not shown. The question arises whether patients who have stool s should receive antibiocultures positive for Aerw tic therapy. Although our study was not designed to answer this question, antibiotic therapy may not be
necessaryfor most patients with Aerommu s. Whether the subset of patients who have a more prolonged illness will benefit from antibiotic therapy warrants further investigation. AcknowledPements We thar& Ann Harada for statistical assistance, Emily Chun for transcriptional assistance, and Dr Howard Minami for advice with project design. The project was funded by The Straub Medical Research and Education Foundation. Mr Leong was supported by the Pacific Health Research Institute Summer Scholarship Program. References Aggar, W. A., McCormick, J. D. & Gut-with, M. J. (1985). Clinical and microbiolonical features of Aeronwnus hvdmph&z-associated diarrhoea. Journal of Clinical M&obiolom. 21. 909-913. Burke, V., Gracey, M.,-Robinson, J., Peck, D., Beaman, J. & Btmdell, C. (1983a). The microbiology of childhood gastroenteritis: ~Aero&nus species and-other infective agents. Journal of Infectious Diseases, 148, 68-74. Burke, V., Robinson, J., Beaman, J., Gracey, M., Lesmana, M., Rockhill, R., Echeverria, P. & Janda, J. M. (1983b). Correlation of enterotoxicity with biotype in Aeromonas spp. Journal of Clinical Microbiology, 18, 119~1200. Echeverria, P., Blacklow, N. R., Sanford, L. B. & Cukor, G. G. (1981). Travelers’ diarrhea among American Peace Corp volunteers in rural Thailand. 3oumal of Infectious Diseases, 143, 767-771. Ewing, W. H. (1986). Edwards and Ewing’s Ident$ication of Enterobactmiaceae, 4th edition. New York: Elsevier Science Publishing Company, pp. 2745. Figura, N., Marri, L., Verdiani, S., Ceccherini, C. & Barben, A. (1986). Prevalence, species differentiation, and toxigenicity of Aeromonas strains in cases of childhood gastroenteritis and in controls. 3ournul of Clinical Microbiology, 23, 595-599. Gracey, M., Burke, V. & Robinson, J. (1982). Aerommasassociated gastroenteritis. Lancet, ii, 1304-1306. Holmberg, S. D., Schell, W. L., Fanning, G. R., Wachsmuth, I. K., Hickman-Brenner, F. W., Blake, P. A., Brenner, D. J. & Farmer, J. J. III (1986). Aeromonas intestinal infections in the United States. Annals of Internal Medicine, 105, 683-689. Morgan, D. R., Johnson, P. C., Cad&l, P., DuPont, H. L., Satterwhite, T. K. & Wood, L. V. (1985). Lack of correlation between known virulence properties of Aeromoms hydrophila and enteropathogenicity for humans. Infection and Immuniry, 50, 62-65. Moyer, N. P. (1987). Clinical significance of Aeronwnas species isolated from patients with diarrhea. 3ournal of Clinical Microbiology, 25, 2044-2048. Pien, F. D., Hsu, A. K., Padua, S. A., Isaacson, N. S. & Naka, S. (1983). Campylobacter jejuni enteritis in Honolulu, Hawaii. Transactions of the Royal Society of Troptcal Medicine and Hygiene, 77, 492-494. Pouoff. M. (1984). Aemmmm. In Bureev’s Manual of ~S$matic‘Bact&ology, vol. l., Krieg, N.< R. & Holt, J. G. (editors). Baltimore: Wilhams and Wilkins, pp. 545-548. Travis, L. B. & Washington, J. A. II (1986). Thisat significance of stool isolates of Amnnona . Journal of Clinical Pathology, 85, 330-336. Watson, I. M., Robinson, J. O., Burke, V. & Gracey, M. (1985). Invasiveness of Aeromonus spp. in relation to biotype, virulence factors, and clinical features. Journ of Clinical Microbiology, 22, 48-51. --I
Received
--I
3 May
August 1989
1989;
accepted
for
publication
15