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Septicaemia due to Yersinia enterocolitica biotype 1 in Hong Kong
Journal of Infection (1984) 8, 28-33
S e p t i c a e m i a d u e to Yer$inia ¢ n t e r o c o l i t i c a b i o t y p e I in H o n g K o n g W. H. Seto* and J. T. K. Laut Departments of *Microbiology and t Surgery, University of Hong Kong Accepted for publication 28 February I983 Summary The clinical histories of four patients with septicaemia due to Yersinia enterocolitica biotype i and the biochemical reactions of the isolates are reported. Three of the isolates were serotype Ol 7 and one was non-typable. These are the first reports of Y. enterocolitica septicaemia from Asia and of septicaemia due to biotype I which has previously been postulated to be non-pathogenic. All four patients had an underlying illness (two with metastatic neoplasms and two with burns). All of the patients recovered fully despite the high mortality associated with this condition. It is postulated that biotype I is of low pathogenicity.
Introduction Yersinia enterocolitica has been implicated as the causative agent of a wide variety of clinical conditions in h u m a n beings including gastroenteritis, mesenteric lymphadenitis, terminal ileitis, arthritis, erythema n o d o s u m , meningitis and septicaemia. T h e most c o m m o n presentation is with gastroenteritis in y o u n g children, b u t in older children and y o u n g adults, abdominal pain due to mesenteric lymphadenitis with or without terminal ileitis is more frequent. 1, ~ Septicaemia due to Y. enterocolitica however is u n c o m m o n . Only a b o u t 55 cases have been reported in the literature, mostly from Europe, N o r t h America and South Africa? This paper, detailing four cases of Y. enterocolitica septicaemia is the first report o f this condition from Asia, where only non-septicaemic cases have been reported before from Japan?. 5 F u r t h e r m o r e , this is p r o b a b l y the first report of septicaemia due to Y. enterocolitica b i o t y p e 1.1 T h i s should help to resolve the controversy over the pathogenic potential of this biotype, which some authors have postulated to be non-pathogenic. 6' 7 Methods In all four patients Y. enterocolitica was isolated in the course of routine laboratory processing of blood cultures. T h e basic b r o t h m e d i u m in our laboratory was brain heart infusion b r o t h for aerobic cultures, s u p p l e m e n t e d with thioglycollate, vitamin K and haemin for anaerobic cultures. Subcultures were m a d e on ' chocolate' and 7 per cent horse blood agar four times extended over a period of weeks and incubated b o t h aerobically and anaerobically in 5-1o per cent carbon dioxide (CO2) for 48 hours. Faecal specimens were inoculated on to M a c C o n k e y and deoxycholate agar before and after cold enrichment. Cultures were incubated at 25 °C and 37 °C for 48 hours. F o r cold enrichment, a portion of the specimen was incubated in a 1/15 M phosphate buffer solution ( p H 7"6) at 4 °C for zo d a y s ? o163-4453/84/OlOO28+o6 $02.oo/0
©1984 The British Society for the Study of Infection
Yersinia enterocolitica septicaemia
29
Identification of Y. enterocolitica was made according to the cultural and biochemical tests for the identification of Enterobacteriaceae. s Antibiotic sensitivities were assessed according to the K i r b y - B a u e r method. Serotyping was kindly done at the Central Public H e a l t h L a b o r a t o r y , Colindale, L o n d o n , where the identities of the isolates were also confirmed. Results Case histories
Patient one A z o - m o n t h - o l d Chinese b o y was scalded b y hot water 4 days before admission. H e was first seen b y a general practitioner w h o applied a local dressing and prescribed oral ampicillin. A few days later, he was referred to hospital with pus discharging from the b u r n t area and a fever of 4o °C. O n admission, the patient had a p u r u l e n t b u r n of the right foot. H i s t e m p e r a t u r e was 38"6 °C. Culture of the pus yielded only Pseudomonas spp., sensitive to gentamicin. T h e white blood cell count ( W B C ) was 14 x lO9/1. After 4 days' incubation the b l o o d culture taken on admission yielded n o n - t y p a b l e Y. enterocolitica b i o t y p e I. T w o stool cultures taken a week later were negative for Yersinia. T h e patient was first given ampicillin and cloxacillin with local antiseptic treatment and repeated dressings with silver sulphadiazine cream. T h r e e days later w h e n the pus cultural result was k n o w n ampicillin and cloxacillin were discontinued. Gentamicin therapy was started and continued for a full week. T h e r e was a good response and the patient was afebrile after a week. H e was transferred to a convalescent ward and was discharged 3 weeks later. Patient two
T h i s Chinese boy, first presented in 1981, w h e n he was 2 m o n t h s old, with a n e u r o b l a s t o m a of the left kidney. It was r e m o v e d surgically in A u g u s t I98I. In J u n e 1982, w h e n a year old, he was readmitted for the investigation of a 3 cm diameter s u b c u t a n e o u s mass located in the left l u m b a r region. N o other abnormalities were f o u n d and he was afebrile. Although no invasive procedures were a t t e m p t e d the patient had a spike of fever of 39"4 °C on the fifth day after admission and a blood culture was taken. T h e W B C was 9"6 x lO9/1 and the patient was treated with analgesics alone. H e continued to have intermittent fever with spikes of t e m p e r a t u r e up to 40 °C. Blood culture yielded Y. enterocolitica b i o t y p e I, serotype o i 7 , after 4 days of incubation. Gentamicin therapy' was b e g u n a week after the fever started. T h e r e was no abdominal discomfort t h r o u g h o u t the illness and repeated stool cultures were negative for Yersinia. T h e fever began to settle after 48 hours of antibiotic therapy b u t he developed a macular rash over the head and trunk which lasted for a few days. D u r i n g the transfer of the patient to another ward, the gentamicin was s t o p p e d after three days of therapy and treatment was changed to ampicillin (to which the organism was resistant in vitro). Nevertheless, the patient continued to improve. H e was afebrile and his b l o o d culture was sterile a few days after the transfer. T h e mass, later shown to be metastatic neuroblastoma, was r e m o v e d and another metastatic s u b c u t a n e o u s mass was excised 2 m o n t h s later. At the time of writing, the patient was well with no further evidence of metastases.
3°
W. H. SETO AND J. T. K. LAU
Patient three A I-year-old Chinese girl was scalded on the day of admission. On examination, she was afebrile with secondary burns over the face, shoulders and upper chest (about i2 per cent of body surface). She was started on treatment with ampicillin and cloxacillin. Silver sulphadiazine cream was applied to the burnt areas. T h e next day, the patient developed a swinging fever of 38"3 °C to 39"4 °C without clinical evidence of infection of the burn or gastrointestinal symptoms. T h e WBC was I5"5 × Io9/1. T h e wound swab taken on admission yielded only Staphylococcus albus. After 4 days of incubation, the blood culture yielded Y. enterocolitica biotype I, serotype oI7, but two stool cultures taken after the latter was reported were both negative for Yersinia. Six days after the onset of fever, the antibiotics were replaced by gentamicin on the basis of the blood culture report. T h e patient improved and was afebrile 48 hours later. Gentamicin was given for two more days. She continued to improve and was discharged ~ weeks later. Patient/our An 89-year-old Chinese woman had presented previously with cervical lymphadenopathy, a ballotable mass in the abdomen and hepatomegaly. L y m p h node biopsy revealed undifferentiated metastatic carcinoma and she was admitted this time in an attempt to locate the primary turnout. Hepatic arteriogram, renal arteriogram, two retrograde pyelograms and a cystoscopy with biopsy were performed. On the day of the second retrograde pyelogram and a week after cystoscopy, her temperature rose to 38"3 °C. T h e WBC was I 1.5 x Io9/1. T h e r e was significant bacteriuria with Proteus mirabilis sensitive to gentamicin. Two blood cultures taken on consecutive days both yielded Y. enterolitica biotype I, serotype o~7, and Alcaligenes faecalis, both of which were sensitive to gentamicin. Cephalexin and gentamicin therapy were started the day after the onset of fever and gentamicin therapy was continued for 9 days while cephalexin therapy was stopped after 3 days when the cultural results were known. After 8 days of intermittent fever (37"7 °C to 38"8 °C) with no other significant signs or symptoms, the patient recovered and became afebrile. Although tumour tissue was found in the urinary tract, it was not possible to ascertain whether the lesions were primary or secondary. She was discharged 6 days after her recovery from the septicaemia and referred for radiotherapy.
Bacteriology T h e biochemical characteristics of the four strains of Y. enterocolitica isolated are shown in Table I. Except for the delay in some positive reactions, results of biochemical tests were similar for all four strains. On the basis of these reactions, the organism falls into biotype I according to the scheme proposed by Nil~hn 9 and Wauters. 1° T h e antimicrobial susceptibility patterns were similar for all isolates except that only the strain isolated from the first patient was susceptible to ampicillin. All four strains were susceptible to cefamandole, tetracycline, co-trimoxazole, gentamicin, kanamycin and chloramphenicol.
Yersinia enterocolitica Table I
septicaemia
Characteristics of the strains of Y e r s i n i a Patient I
Motility 25 °C 37 °C Voges-Proskauer 25 °C 37 °C O / F medium Catalase Indole Methyl Red Nitrate Reduction Urease Aesculin hydrolysis fl-Galactosidase Ornithine decarboxylase Lecithinase production (25 °C) Lysine decarboxylase Arginine dihydrolase Phenylalanine deaminase H2S ( T S I ) Citrate (Simmons) Oxidase Sugar Fermentation Results Glucose Lactose Maltose Mannitol Sucrose Arabinose Salicin Sorbitol Rhamnose Melibiose Raffinose Xylose Ducitol Adonitol
+ . + . F + + + + + + + + (+) . . . . . . + + + + + + + + + +1 +x +2 . .
3I
enterocolitica
Patient 2
Patient 3
Patient 4
+
+
+ .
.
. +
+
.
. F + + + (+) + + + + (+ )
. . . . . .
F + + + (+) + + + + (+ ) . . . . . .
+ (+ ) + + + + + + + +2 +2 +
. .
+ (+ ) + + (+ ) + + + + +2 +~ +2 . .
+ . F + + + + + + + + (+ ) . . . . . . + (+ ) + + + + + + + +2 +2 +2 . .
isolated
F = fermentative; + -- positive within 24 hours; ( + ) = positive between 24 and 48 hours; + 1 = positive between 48 and 72 hours; + 2 = positive between 3 and 7 days.
Discussion
Yersinia enterocolitica c a u s e s s e v e r a l h u m a n d i s e a s e s b u t it is n o t c e r t a i n w h e t h e r all b i o t y p e s a r e p a t h o g e n i c . 1 A n u m b e r o f d i f f e r e n t s c h e m e s f o r biotyping exist, although those of Nil6hn and Wauters are the most commonly used. 1 Based on this scheme of biotyping, Noyen and colleagues 6 postulated, after an 8-year survey and analysis of 2Iz isolates (nine of which were biotype I ) , t h a t b i o t y p e I is p r o b a b l y n o n - p a t h o g e n i c i n B e l g i u m . E i g h t o f n i n e p a t i e n t s were asymptomatic and no agglutinins against his own organism were found in
32
w. H. SETO AND J. T. K. LA
the ninth patient who presented with an appendicular syndrome. Similar conclusions were reached independently by French workers. 7 Isolation of biotype I from the stools of patients with gastroenteritis has been reported from Canada, 11 South Africa 12 and the U.S.A., 13,14 although the relationship between the organism and the disease is not certain as the isolates were only from the stool. T h e organisms isolated in our four patients who were clinically septicaemic were from the blood and this strongly supports the belief that Y . enterocolitica biotype I is pathogenic for human beings. Although biotype I caused septicaemia in our patients, the pathogenicity of this organism is probably low. All of our patients survived even though this condition has been associated with a high mortality. 3 It should also be noted that patients two and three who only had three and four days respectively of appropriate antibiotic therapy also recovered fully. Yersinia enterocolitica septicaemia generally affects patients with underlying illness. 3 This was so in all of our patients but the underlying diseases were not those frequently associated with this type of septicaemia. Among 55 cases reviewed by Bouza and colleaguesfl only four had underlying neoplasms (bowel carcinoma, hepatoma, lymphoma, and leukaemia)3; none had burns. In contrast, two of our patients had metastatic neoplasms and two had burns. Other clinical and laboratory observations associated with our patients have been reported before. T h e antibiotic sensitivity pattern, with good susceptibility to aminoglycosides and resistance to ampicillin correlates well with other studies.15,16 Although the absence of abdominal signs and symptoms in our patients is unusual, 17 several patients with a similar clinical presentation have been reported before in the literature. 3, 18-20Negative stool cultures in patients with Y . enterocolitica septicaemia, have also been described elsewhere.3,17,19.21, 22 We are uncertain as to the source of infection and the pathogenesis of the septicaemia in our patients. None of the patients kept pets in their homes. T h e three children were from the same ward but stool cultures of I5 of the ward staff and swabs of the bath tubs and towels were all negative for Y. enterocolitica.
T h e isolation of Y . enterocolitica from the stool has not previously been reported in Hong Kong. Further studies in the form of screening surveys or the taking of appropriate stool cultures from symptomatic patients may increase our understanding of Yersiniosis in this community. The authors would like to thank the staff of the Central Public Health Laboratory, Colindale, London, for their kind assistance. References I. WeissfeldAS. Yersinia enterocolitica. Clin Microbiol Newslett I98I ; 3: 91-93. 2. RabsonAR, Hallett AF, KoornhofHJ. Generalised Yersinia enterocolitica infection.J Infect Dis I975; I3I: 447-45I. 3. Bouza E, Dominguez A, Meseguer Met al. Yersinia enterocolitica septicemia. Am J Clin Pathol I98O; 74: 404-409. 4. Zen-Yoji H, Maruyama T. The first successful isolation and identification of Yersinia enterocolitica from human cases in Japan. Japan J Microbiol I972; I6: 493-500.
Yersinia enterocolitica
septicaemia
33
5. Asakawa Y, Akahane S, Kagata N, Noguchi M, Sakarzaki R, Tamura K. Two community outbreaks of human infection with Yersinia enterocolitica. J Hyg 1973; 7I : 715-723. 6. Noyen van R, Vandepitte J, Wauters G. Nonvalue of cold enrichment of stools for isolation of Yersina enterocolitica serotypes 3 and 9 from patients. J Clin Microbiol 1980; 1 I : 127-I 3 I. 7. Thibault M, Duval J. Recherche syst~matiqu6 de Yersinia en. Chezl'homme en region parisienne. Med Mal Infect 1978; 8: 691-694. 8. Martin WJ, Washington JA. Enterobactericeae. In: Lennette EH, ed. Manual of Clinical Microbiology, 3rd Edition. Washington, D.C. : A S M , 198o: 195-219. 9. Nil6hn B. Studies on Yersinia enterocolitica with special reference to bacterial diagnosis and occurence in human acute enteric disease. Acta Pathol Microbiol Scand (suppl.) 1969; 206: 1-48. IO. Wauters G. Contribution a l'etude de Yersinia enterocolitica, Thesis. Vander Ed., Louvain, 197o. I I . Marks M I , Pal CH, Lafleur L, Lackman L, Hammerberg O. Yersinia enterocolitica gastroenteritis: A prospective study of clinical, bacteriologic, and epidemiologic features. J Pediatr 198o; 96 26-31. 12. Robins-Browne RM, Jacobs MR, Koornhof HJ, Mauff AC. Yersinia enterocolitica biotype I in South Africa. S Afr M e d J 1979; 55: lO57-1o59. 13. Black RE, Jackson RJ, Tsai T et al. Epidemic Yersinia enterocolitica infection due to contaminated chocolate milk. N Eng J Med 1978, 298 : 76-79. 14. Weissfeld AS, Sonnenwirth AC. Yersinia enterocolitica in adults with gastrointestinal disturbances: Need for cold enrichment. J Clin Microbiol 198o; 11: 196-197. 15. Bissett M. Yersinia enterocolitica isolates from humans in California 1968-1975. J Clin Microbiol 1976; 4: 137-144. 16. Bottone FJ. Yersinia enterocolitica: a panoramic view of a charismatic organism. CRC Crit Rev Microbiol 1977; 5 : 211-214. 17. Caplan L M , Dobson M L , Dorkin H. Yersinia enterocolitica septicaemia. Am J Clin Pathol 1978; 69: 189-192. 18. Josefsson K, Lindberg A. Yersinia enterocolitica septicemia. ScandJ Infect Dis 1975; 7: 76-77. 19. Spira TJ, Kabins SA. Yersinia enterocolitica septicemia with septic arthritis. Arch Intern Med 1977; 136: 13o5-13o8. 2o. Taylor BG, Zafarzai M Z , Humphreys D W , Manfredi F. Nodular pulmonary infiltrates and septic arthritis associated with Yersinia enterocolitica bacteremia. Am Rev Resp Dis 1977; I16: 525-529. 21. Hewstone AS, Davidson GP. Yersinia enterocolitica septicaemia with arthritis in a thalassaemic child. M e d J Aust 1972; 1 lO35-1o38. 22. Mantse L, West J, Cosman H H , Mullens JE. Liver abscess due to Yersinia enterocolitica. C M A J 1978; 119: 922-923. 23. Groote de G, Vandepitte J, Wauters G. Surveillance of human Yersinia enterocolitiea infections in Belgium: 1963-1978. J Infect 1982; 4: 189-197.
2
JIlq S
S e p t i c a e m i a d u e to Yer$inia ¢ n t e r o c o l i t i c a b i o t y p e I in H o n g K o n g W. H. Seto* and J. T. K. Laut Departments of *Microbiology and t Surgery, University of Hong Kong Accepted for publication 28 February I983 Summary The clinical histories of four patients with septicaemia due to Yersinia enterocolitica biotype i and the biochemical reactions of the isolates are reported. Three of the isolates were serotype Ol 7 and one was non-typable. These are the first reports of Y. enterocolitica septicaemia from Asia and of septicaemia due to biotype I which has previously been postulated to be non-pathogenic. All four patients had an underlying illness (two with metastatic neoplasms and two with burns). All of the patients recovered fully despite the high mortality associated with this condition. It is postulated that biotype I is of low pathogenicity.
Introduction Yersinia enterocolitica has been implicated as the causative agent of a wide variety of clinical conditions in h u m a n beings including gastroenteritis, mesenteric lymphadenitis, terminal ileitis, arthritis, erythema n o d o s u m , meningitis and septicaemia. T h e most c o m m o n presentation is with gastroenteritis in y o u n g children, b u t in older children and y o u n g adults, abdominal pain due to mesenteric lymphadenitis with or without terminal ileitis is more frequent. 1, ~ Septicaemia due to Y. enterocolitica however is u n c o m m o n . Only a b o u t 55 cases have been reported in the literature, mostly from Europe, N o r t h America and South Africa? This paper, detailing four cases of Y. enterocolitica septicaemia is the first report o f this condition from Asia, where only non-septicaemic cases have been reported before from Japan?. 5 F u r t h e r m o r e , this is p r o b a b l y the first report of septicaemia due to Y. enterocolitica b i o t y p e 1.1 T h i s should help to resolve the controversy over the pathogenic potential of this biotype, which some authors have postulated to be non-pathogenic. 6' 7 Methods In all four patients Y. enterocolitica was isolated in the course of routine laboratory processing of blood cultures. T h e basic b r o t h m e d i u m in our laboratory was brain heart infusion b r o t h for aerobic cultures, s u p p l e m e n t e d with thioglycollate, vitamin K and haemin for anaerobic cultures. Subcultures were m a d e on ' chocolate' and 7 per cent horse blood agar four times extended over a period of weeks and incubated b o t h aerobically and anaerobically in 5-1o per cent carbon dioxide (CO2) for 48 hours. Faecal specimens were inoculated on to M a c C o n k e y and deoxycholate agar before and after cold enrichment. Cultures were incubated at 25 °C and 37 °C for 48 hours. F o r cold enrichment, a portion of the specimen was incubated in a 1/15 M phosphate buffer solution ( p H 7"6) at 4 °C for zo d a y s ? o163-4453/84/OlOO28+o6 $02.oo/0
©1984 The British Society for the Study of Infection
Yersinia enterocolitica septicaemia
29
Identification of Y. enterocolitica was made according to the cultural and biochemical tests for the identification of Enterobacteriaceae. s Antibiotic sensitivities were assessed according to the K i r b y - B a u e r method. Serotyping was kindly done at the Central Public H e a l t h L a b o r a t o r y , Colindale, L o n d o n , where the identities of the isolates were also confirmed. Results Case histories
Patient one A z o - m o n t h - o l d Chinese b o y was scalded b y hot water 4 days before admission. H e was first seen b y a general practitioner w h o applied a local dressing and prescribed oral ampicillin. A few days later, he was referred to hospital with pus discharging from the b u r n t area and a fever of 4o °C. O n admission, the patient had a p u r u l e n t b u r n of the right foot. H i s t e m p e r a t u r e was 38"6 °C. Culture of the pus yielded only Pseudomonas spp., sensitive to gentamicin. T h e white blood cell count ( W B C ) was 14 x lO9/1. After 4 days' incubation the b l o o d culture taken on admission yielded n o n - t y p a b l e Y. enterocolitica b i o t y p e I. T w o stool cultures taken a week later were negative for Yersinia. T h e patient was first given ampicillin and cloxacillin with local antiseptic treatment and repeated dressings with silver sulphadiazine cream. T h r e e days later w h e n the pus cultural result was k n o w n ampicillin and cloxacillin were discontinued. Gentamicin therapy was started and continued for a full week. T h e r e was a good response and the patient was afebrile after a week. H e was transferred to a convalescent ward and was discharged 3 weeks later. Patient two
T h i s Chinese boy, first presented in 1981, w h e n he was 2 m o n t h s old, with a n e u r o b l a s t o m a of the left kidney. It was r e m o v e d surgically in A u g u s t I98I. In J u n e 1982, w h e n a year old, he was readmitted for the investigation of a 3 cm diameter s u b c u t a n e o u s mass located in the left l u m b a r region. N o other abnormalities were f o u n d and he was afebrile. Although no invasive procedures were a t t e m p t e d the patient had a spike of fever of 39"4 °C on the fifth day after admission and a blood culture was taken. T h e W B C was 9"6 x lO9/1 and the patient was treated with analgesics alone. H e continued to have intermittent fever with spikes of t e m p e r a t u r e up to 40 °C. Blood culture yielded Y. enterocolitica b i o t y p e I, serotype o i 7 , after 4 days of incubation. Gentamicin therapy' was b e g u n a week after the fever started. T h e r e was no abdominal discomfort t h r o u g h o u t the illness and repeated stool cultures were negative for Yersinia. T h e fever began to settle after 48 hours of antibiotic therapy b u t he developed a macular rash over the head and trunk which lasted for a few days. D u r i n g the transfer of the patient to another ward, the gentamicin was s t o p p e d after three days of therapy and treatment was changed to ampicillin (to which the organism was resistant in vitro). Nevertheless, the patient continued to improve. H e was afebrile and his b l o o d culture was sterile a few days after the transfer. T h e mass, later shown to be metastatic neuroblastoma, was r e m o v e d and another metastatic s u b c u t a n e o u s mass was excised 2 m o n t h s later. At the time of writing, the patient was well with no further evidence of metastases.
3°
W. H. SETO AND J. T. K. LAU
Patient three A I-year-old Chinese girl was scalded on the day of admission. On examination, she was afebrile with secondary burns over the face, shoulders and upper chest (about i2 per cent of body surface). She was started on treatment with ampicillin and cloxacillin. Silver sulphadiazine cream was applied to the burnt areas. T h e next day, the patient developed a swinging fever of 38"3 °C to 39"4 °C without clinical evidence of infection of the burn or gastrointestinal symptoms. T h e WBC was I5"5 × Io9/1. T h e wound swab taken on admission yielded only Staphylococcus albus. After 4 days of incubation, the blood culture yielded Y. enterocolitica biotype I, serotype oI7, but two stool cultures taken after the latter was reported were both negative for Yersinia. Six days after the onset of fever, the antibiotics were replaced by gentamicin on the basis of the blood culture report. T h e patient improved and was afebrile 48 hours later. Gentamicin was given for two more days. She continued to improve and was discharged ~ weeks later. Patient/our An 89-year-old Chinese woman had presented previously with cervical lymphadenopathy, a ballotable mass in the abdomen and hepatomegaly. L y m p h node biopsy revealed undifferentiated metastatic carcinoma and she was admitted this time in an attempt to locate the primary turnout. Hepatic arteriogram, renal arteriogram, two retrograde pyelograms and a cystoscopy with biopsy were performed. On the day of the second retrograde pyelogram and a week after cystoscopy, her temperature rose to 38"3 °C. T h e WBC was I 1.5 x Io9/1. T h e r e was significant bacteriuria with Proteus mirabilis sensitive to gentamicin. Two blood cultures taken on consecutive days both yielded Y. enterolitica biotype I, serotype o~7, and Alcaligenes faecalis, both of which were sensitive to gentamicin. Cephalexin and gentamicin therapy were started the day after the onset of fever and gentamicin therapy was continued for 9 days while cephalexin therapy was stopped after 3 days when the cultural results were known. After 8 days of intermittent fever (37"7 °C to 38"8 °C) with no other significant signs or symptoms, the patient recovered and became afebrile. Although tumour tissue was found in the urinary tract, it was not possible to ascertain whether the lesions were primary or secondary. She was discharged 6 days after her recovery from the septicaemia and referred for radiotherapy.
Bacteriology T h e biochemical characteristics of the four strains of Y. enterocolitica isolated are shown in Table I. Except for the delay in some positive reactions, results of biochemical tests were similar for all four strains. On the basis of these reactions, the organism falls into biotype I according to the scheme proposed by Nil~hn 9 and Wauters. 1° T h e antimicrobial susceptibility patterns were similar for all isolates except that only the strain isolated from the first patient was susceptible to ampicillin. All four strains were susceptible to cefamandole, tetracycline, co-trimoxazole, gentamicin, kanamycin and chloramphenicol.
Yersinia enterocolitica Table I
septicaemia
Characteristics of the strains of Y e r s i n i a Patient I
Motility 25 °C 37 °C Voges-Proskauer 25 °C 37 °C O / F medium Catalase Indole Methyl Red Nitrate Reduction Urease Aesculin hydrolysis fl-Galactosidase Ornithine decarboxylase Lecithinase production (25 °C) Lysine decarboxylase Arginine dihydrolase Phenylalanine deaminase H2S ( T S I ) Citrate (Simmons) Oxidase Sugar Fermentation Results Glucose Lactose Maltose Mannitol Sucrose Arabinose Salicin Sorbitol Rhamnose Melibiose Raffinose Xylose Ducitol Adonitol
+ . + . F + + + + + + + + (+) . . . . . . + + + + + + + + + +1 +x +2 . .
3I
enterocolitica
Patient 2
Patient 3
Patient 4
+
+
+ .
.
. +
+
.
. F + + + (+) + + + + (+ )
. . . . . .
F + + + (+) + + + + (+ ) . . . . . .
+ (+ ) + + + + + + + +2 +2 +
. .
+ (+ ) + + (+ ) + + + + +2 +~ +2 . .
+ . F + + + + + + + + (+ ) . . . . . . + (+ ) + + + + + + + +2 +2 +2 . .
isolated
F = fermentative; + -- positive within 24 hours; ( + ) = positive between 24 and 48 hours; + 1 = positive between 48 and 72 hours; + 2 = positive between 3 and 7 days.
Discussion
Yersinia enterocolitica c a u s e s s e v e r a l h u m a n d i s e a s e s b u t it is n o t c e r t a i n w h e t h e r all b i o t y p e s a r e p a t h o g e n i c . 1 A n u m b e r o f d i f f e r e n t s c h e m e s f o r biotyping exist, although those of Nil6hn and Wauters are the most commonly used. 1 Based on this scheme of biotyping, Noyen and colleagues 6 postulated, after an 8-year survey and analysis of 2Iz isolates (nine of which were biotype I ) , t h a t b i o t y p e I is p r o b a b l y n o n - p a t h o g e n i c i n B e l g i u m . E i g h t o f n i n e p a t i e n t s were asymptomatic and no agglutinins against his own organism were found in
32
w. H. SETO AND J. T. K. LA
the ninth patient who presented with an appendicular syndrome. Similar conclusions were reached independently by French workers. 7 Isolation of biotype I from the stools of patients with gastroenteritis has been reported from Canada, 11 South Africa 12 and the U.S.A., 13,14 although the relationship between the organism and the disease is not certain as the isolates were only from the stool. T h e organisms isolated in our four patients who were clinically septicaemic were from the blood and this strongly supports the belief that Y . enterocolitica biotype I is pathogenic for human beings. Although biotype I caused septicaemia in our patients, the pathogenicity of this organism is probably low. All of our patients survived even though this condition has been associated with a high mortality. 3 It should also be noted that patients two and three who only had three and four days respectively of appropriate antibiotic therapy also recovered fully. Yersinia enterocolitica septicaemia generally affects patients with underlying illness. 3 This was so in all of our patients but the underlying diseases were not those frequently associated with this type of septicaemia. Among 55 cases reviewed by Bouza and colleaguesfl only four had underlying neoplasms (bowel carcinoma, hepatoma, lymphoma, and leukaemia)3; none had burns. In contrast, two of our patients had metastatic neoplasms and two had burns. Other clinical and laboratory observations associated with our patients have been reported before. T h e antibiotic sensitivity pattern, with good susceptibility to aminoglycosides and resistance to ampicillin correlates well with other studies.15,16 Although the absence of abdominal signs and symptoms in our patients is unusual, 17 several patients with a similar clinical presentation have been reported before in the literature. 3, 18-20Negative stool cultures in patients with Y . enterocolitica septicaemia, have also been described elsewhere.3,17,19.21, 22 We are uncertain as to the source of infection and the pathogenesis of the septicaemia in our patients. None of the patients kept pets in their homes. T h e three children were from the same ward but stool cultures of I5 of the ward staff and swabs of the bath tubs and towels were all negative for Y. enterocolitica.
T h e isolation of Y . enterocolitica from the stool has not previously been reported in Hong Kong. Further studies in the form of screening surveys or the taking of appropriate stool cultures from symptomatic patients may increase our understanding of Yersiniosis in this community. The authors would like to thank the staff of the Central Public Health Laboratory, Colindale, London, for their kind assistance. References I. WeissfeldAS. Yersinia enterocolitica. Clin Microbiol Newslett I98I ; 3: 91-93. 2. RabsonAR, Hallett AF, KoornhofHJ. Generalised Yersinia enterocolitica infection.J Infect Dis I975; I3I: 447-45I. 3. Bouza E, Dominguez A, Meseguer Met al. Yersinia enterocolitica septicemia. Am J Clin Pathol I98O; 74: 404-409. 4. Zen-Yoji H, Maruyama T. The first successful isolation and identification of Yersinia enterocolitica from human cases in Japan. Japan J Microbiol I972; I6: 493-500.
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5. Asakawa Y, Akahane S, Kagata N, Noguchi M, Sakarzaki R, Tamura K. Two community outbreaks of human infection with Yersinia enterocolitica. J Hyg 1973; 7I : 715-723. 6. Noyen van R, Vandepitte J, Wauters G. Nonvalue of cold enrichment of stools for isolation of Yersina enterocolitica serotypes 3 and 9 from patients. J Clin Microbiol 1980; 1 I : 127-I 3 I. 7. Thibault M, Duval J. Recherche syst~matiqu6 de Yersinia en. Chezl'homme en region parisienne. Med Mal Infect 1978; 8: 691-694. 8. Martin WJ, Washington JA. Enterobactericeae. In: Lennette EH, ed. Manual of Clinical Microbiology, 3rd Edition. Washington, D.C. : A S M , 198o: 195-219. 9. Nil6hn B. Studies on Yersinia enterocolitica with special reference to bacterial diagnosis and occurence in human acute enteric disease. Acta Pathol Microbiol Scand (suppl.) 1969; 206: 1-48. IO. Wauters G. Contribution a l'etude de Yersinia enterocolitica, Thesis. Vander Ed., Louvain, 197o. I I . Marks M I , Pal CH, Lafleur L, Lackman L, Hammerberg O. Yersinia enterocolitica gastroenteritis: A prospective study of clinical, bacteriologic, and epidemiologic features. J Pediatr 198o; 96 26-31. 12. Robins-Browne RM, Jacobs MR, Koornhof HJ, Mauff AC. Yersinia enterocolitica biotype I in South Africa. S Afr M e d J 1979; 55: lO57-1o59. 13. Black RE, Jackson RJ, Tsai T et al. Epidemic Yersinia enterocolitica infection due to contaminated chocolate milk. N Eng J Med 1978, 298 : 76-79. 14. Weissfeld AS, Sonnenwirth AC. Yersinia enterocolitica in adults with gastrointestinal disturbances: Need for cold enrichment. J Clin Microbiol 198o; 11: 196-197. 15. Bissett M. Yersinia enterocolitica isolates from humans in California 1968-1975. J Clin Microbiol 1976; 4: 137-144. 16. Bottone FJ. Yersinia enterocolitica: a panoramic view of a charismatic organism. CRC Crit Rev Microbiol 1977; 5 : 211-214. 17. Caplan L M , Dobson M L , Dorkin H. Yersinia enterocolitica septicaemia. Am J Clin Pathol 1978; 69: 189-192. 18. Josefsson K, Lindberg A. Yersinia enterocolitica septicemia. ScandJ Infect Dis 1975; 7: 76-77. 19. Spira TJ, Kabins SA. Yersinia enterocolitica septicemia with septic arthritis. Arch Intern Med 1977; 136: 13o5-13o8. 2o. Taylor BG, Zafarzai M Z , Humphreys D W , Manfredi F. Nodular pulmonary infiltrates and septic arthritis associated with Yersinia enterocolitica bacteremia. Am Rev Resp Dis 1977; I16: 525-529. 21. Hewstone AS, Davidson GP. Yersinia enterocolitica septicaemia with arthritis in a thalassaemic child. M e d J Aust 1972; 1 lO35-1o38. 22. Mantse L, West J, Cosman H H , Mullens JE. Liver abscess due to Yersinia enterocolitica. C M A J 1978; 119: 922-923. 23. Groote de G, Vandepitte J, Wauters G. Surveillance of human Yersinia enterocolitiea infections in Belgium: 1963-1978. J Infect 1982; 4: 189-197.
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