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Characteristics of Bacteremia Between Community-Acquired and Nosocomial Klebsiella pneumoniae Infection
Risk Factor for Mortality and the Impact of Capsular Serotypes as a Herald for Community-Acquired Infection
Ren-Wen Tsay, MD;
L. K. Siu, PhD;
Chang-Phone Fung, MD;
Feng-Yee Chang, MD, PhD
Arch Intern Med. 2002;162:1021-1027.
ABSTRACT
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Background Although several epidemiological surveys of Klebsiella clinical isolates have been performed, few studies have correlated
the clinical isolate with disease.
Objective To compare the clinical and bacteriological characteristics of Klebsiella pneumoniae bacteremia acquired as community
or nosocomial infections.
Methods We prospectively enrolled 158 consecutively hospitalized patients with K pneumoniae bacteremia. Clinical data were reviewed. Antimicrobial
susceptibility testing and capsular serotyping were performed. We used the  2 test, the Fisher exact test, or the t test
for statistic analysis.
Results Underlying diabetes mellitus was more common in community-acquired than
in nosocomial infection (46/94 [49%] vs 8/64 [12%]; P<.001).
On the other hand, neoplastic disease (34/64 [53%] vs 13/94 [14%]; P<.001) and antibiotic resistance (P<.01)
were more frequent in patients with nosocomial compared with community-acquired
infections. Klebsiella pneumoniae liver abscesses,
which were all community acquired, accounted for the source of 22 (23%) of
94 community-acquired K pneumoniae infections. No
attributable source of infection was found for 37 (58%) of the 64 nosocomial
infections vs 15 (16%) of the 94 community-acquired infections. Only 58 isolates
(36.7%) could be serotyped; of these, capsular serotypes K1, K2, and K28 accounted
for 37 (23.4%), 8 (5.1%), and 6 (3.8%), respectively, of all strains. However,
typeable isolates were significantly more common among community-acquired
than nosocomial isolates (42/94 [45%] vs 16/64 [25%]; P = .01), especially for serotype K1 (28/94 [30%] vs 9/64 [14%]; P = .02). Significant risk factors for mortality included
nosocomial infection, lung infection, thrombocytopenia, leukopenia, ceftazidime
resistance, inappropriate antimicrobial therapy, and septic shock.
Conclusions Significant differences were identified between community-acquired and
nosocomial K pneumoniae bacteremia. Ceftazidime resistance
in nosocomial K pneumoniae bacteremia carried a high
risk for mortality, and serotype K1 in K pneumoniae
was more prevalent in community-acquired infection, suggesting more virulence.
INTRODUCTION
KLEBSIELLA PNEUMONIAE causes suppurative infections,
bacteremia, and a substantial percentage of nosocomal infections. It is the
second most common cause of gram-negative bacteremia.1-3
Strains of K pneumoniae that are resistant to multiple
antibiotics, including the newer cephalosporins, have developed.4
Infections caused by these extended-spectrum  -lactamase–producing K pneumoniae are frequently epidemic in nature and have
complicated chemotherapy significantly.4-6
Most clinical isolates of K pneumoniae possess a
well-defined polysaccharide capsule that appears to be a critical virulence
factor.7-8 Although several seroepidemiological
surveys of Klebsiella clinical isolates have been
performed,9-12
few studies have correlated the clinical isolate with disease.9-10
Some capsular serotypes are isolated at significantly higher frequency than
others.12-13 We conducted this
study to compare the clinical and bacteriological characteristics of K pneumoniae bacteremia acquired as community or nosocomial
infection.
MATERIALS AND METHODS
DURATION OF STUDY
From April 1, 1997, through March 31, 1999, patients with a blood culture
positive for K pneumoniae at the Tri-Service General
Hospital, a 1300-bed university hospital in Taipei, Taiwan, were prospectively
enrolled. The clinical features of these patients and the bacteriological
characteristics of these K pneumoniae strains were
collected and analyzed.
DEFINITIONS
Klebsiella pneumoniae bacteremia was defined
as the isolation of K pneumoniae in 1 or more blood
cultures in association with the clinical features of bacteremia and/or sepsis.
Bacteremia was considered to be nosocomial if a blood culture that yielded
positive findings was obtained later than 72 hours after admission, and if
the bacteremia was not obviously associated with the clinical conditions of
the patient at the time of admission. Otherwise, bacteremia was considered
to be community acquired.
Previous corticosteroid treatment was defined as corticosteroid therapy
for at least 2 weeks before the onset of the K pneumoniae bacteremia. Recent surgery was defined as a surgical procedure that
had been performed within 1 month of the onset of K pneumoniae bacteremia. The source of bacteremia was defined clinically or by
the isolation of K pneumoniae from the site of entry
or both. An infiltrate had to be seen on the chest radiograph to substantiate
the presence of pneumonia.
Shock was defined as a decrease in systolic blood pressure to a level
of less than 90 mm Hg or a decrease of at least 40 mm Hg below baseline blood
pressure, despite adequate fluid resuscitation, in conjunction with organ
dysfunction and perfusion abnormalities (eg, lactic acidosis, oliguria, obtundation).
Jaundice was defined as a total serum bilirubin level of at least 2.0 mg/dL
( 34.2 µmol/L).
Leukocytosis was defined as a white blood cell count of greater than
10 000/µL; leukopenia, a white blood cell count of less than 4000/µL;
and thrombocytopenia, a platelet count of less than 100 000/µL.
ANTIMICROBIAL THERAPY
Antimicrobial therapy was considered to be appropriate if 1 or more
antimicrobial agents were active in vitro against the corresponding isolate
when the agent(s) was given at an adequate dosage via an appropriate route
for at least 2 days within 3 days of obtaining a blood culture that yielded
positive results. Mortality was considered to be related to bacteremia if
the patient was being treated for bacteremia when death occurred, unless clinical
and pathological data clearly suggested otherwise.
BACTERIAL ISOLATES AND ANTIMICROBIAL SUSCEPTIBILITY TESTING
All isolates were identified by means of the API 20E system (bioMérieux
SA, Marcy I'Etoile, France). Antimicrobial susceptibilities were determined
by means of the Kirby-Bauer disk-diffusion test on Mueller-Hinton agar (BBL
Microbiologic System, Cockeysville, Md) for the following antibiotics: ampicillin
(10 µg), amikacin (30 µg), aztreonam (30 µg), cefazolin
(30 µg), cefuroxime (30 µg), ceftriaxone (30 µg), ceftazidime
(30 µg), ciprofloxacin (30 µg), gentamicin (10 µg), imipenem
(30 µg), piperacillin (100 µg), and a combination of trimethoprim
and sulfamethoxazole (1.25 µg and 23.75 µg, respectively). Interpretations
were performed according to the guidelines of the National Committee for Clinical
Laboratory Standards.14
CAPSULAR SEROTYPE
The isolates were serotyped by means of the countercurrent immunoelectrophoresis
method.15 Antisera were provided by the Laboratory
of Hospital Infection, Central Public Health Laboratory, London, England.
In brief, strains to be serotyped were grown overnight on MacConkey agar (Difco
Laboratories, Detroit, Mich), and a light suspension of bacteria was resuspended
in isotonic sodium chloride solution with different antisera. Each isolate
was tested against 14 antiserum pools by means of countercurrent immunoelectrophoresis
and then tested again with the specific antisera of the reacting pool. Isolates
were examined by means of the quellung (capsular swelling) reaction with antisera
if cross-reactions occurred or if equivocal results were obtained by means
of countercurrent immunoelectrophoresis. Isolates that failed to react in
both methods were considered nontypeable. Klebsiella pneumoniae ATCC 9997 (K2, where K indicates capsular serotype) was used as a
control strain.
The severity of illness was evaluated by means of the APACHE III (Acute
Physiology and Chronic Health Evaluation III) score system.16
STATISTICAL ANALYSIS
We performed statistical analysis using the 2 test,
the Fisher exact test, or the t test. When the P value was less than .05, the difference was considered
statistically significant.
RESULTS
UNDERLYING CONDITIONS
During the 2-year study, 158 patients with an episode of K pneumoniae bacteremia were prospectively enrolled. Ninety-four episodes
(59.5%) were community acquired, and 64 (40.5%) were nosocomial in origin
(Table 1). The ages of patients
ranged from 25 weeks to 90 years (mean ± SD age, 60 ± 19 years).
The male-female ratio was 1.4:1.
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Table 1. Significant Difference Between Community-Acquired and Nosocomial Klebsiella pneumoniae Bacteremia Among Various Underlying
Conditions*
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The common underlying diseases associated with community-acquired K pneumoniae bacteremia were diabetes mellitus (n = 46
[49%]), hepatobiliary disease (n = 29 [31%]), and neoplastic diseases (n =
13 [14%]). The common underlying diseases associated with nosocomial K pneumoniae bacteremia were neoplastic diseases (n = 34
[53%]), hepatobiliary diseases (n = 14 [22%]), and diabetes mellitus (n =
8 [12%]). Underlying diabetes mellitus was more common in community-acquired
than in nosocomial infection (49% vs 12%; P<.001).
Neoplastic disease was more frequently noted in patients with nosocomial compared
with community-acquired infection (53% vs 14%; P<.001; Table 1).
CLINICAL FEATURES AND TREATMENT OF THE ENROLLED PATIENTS
In the nosocomial K pneumoniae bacteremia group,
15 patients (23%) had indwelling urinary catheters or had undergone recent
urinary manipulations. Eleven patients (17%) were receiving immunosuppressive
therapy, including chemotherapy for neoplastic diseases (n = 9) and corticosteroid
treatment (n = 2). Five of 11 patients with bacteremia who required respiratory
assistance had pneumonia. Of the 37 patients with an unknown source of nosocomial
bacteremia, 5 patients had a central venous catheter in place, 2 were receiving
corticosteroid therapy, 6 were receiving chemotherapy, 2 had a central venous
catheter and had undergone recent abdominal surgery, and 1 had undergone recent
abdominal surgery. All of these predisposing factors were found more frequently
in patients with nosocomial bacteremia (P = .01; Table 2).
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Table 2. Significant Difference Between Community-Acquired and Nosocomial Klebsiella pneumoniae Bacteremia Among Predisposing Factor,
Source of Infection, and Clinical Finding*
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For infection origin, intra-abdominal (P<.001)
and urinary tract (P = .01) infections were significantly
higher in community-acquired bacteremia. On the contrary, patients with an
unknown origin of infection had a significantly higher incidence of nosocomial
than community-acquired bacteremia (P<.001; Table 2).
Shock developed in 34 (21.5%) of 158 patients. Twenty patients (12.7%)
displayed leukopenia. Of these, 10 (50.0%) had received chemotherapy for underlying
hematologic neoplasms. Of the patients with leukopenia, 2 had undergone radiotherapy,
4 had cirrhosis of liver, 1 had aplastic anemia, and 3 had no underlying condition.
One hundred eight patients (68.4%) showed leukocytosis. Sixty patients (38.0%)
showed thrombocytopenia. Thirty patients (19.0%) had jaundice. The APACHE
III score was higher in patients with nosocomial infections compared with
those with community-acquired K pneumoniae bacteremia
(mean ± SD score, 41 ± 24 vs 33 ± 21; P = .03). The overall mortality rate was 22.8% (36/158 patients). The
mortality rate was higher in patients with nosocomial infections compared
with those with community-acquired infections (36% vs 14%; P = .001) (Table 2). No
significant differences between community-acquired and nosocomial bacteremia
were observed in corticosteroid use, lung infection, leukocytosis, thrombocytopenia,
creatinine levels of at least 2 mg/dL (176.8 µmol/L), ceftazidime
resistance, inappropriate antibiotic therapy, metastatic foci, and shock.
PATIENTS WITH POLYMICROBIAL INFECTION AND ANTIMICROBIAL SUSCEPTIBILITY
TESTING
Of the 158 patients, 21 (13.3%) were identified as having polymicrobial
bacteremia. The concomitant organisms were Enterococcus (n = 7), Enterobacter cloacae (n = 4), Proteus mirabilis (n = 3), Escherichia
coli (n = 3), methicillin-sensitive Staphylococcus
aureus (n = 2), Pseudomonas aeruginosa (n
= 1), Serratia marcescens (n = 1), Bacteroides species (n = 1), Streptococcus pneumoniae (n = 1), Enterobacter gergoviae (n = 1),
and Citrobacter freundii (n = 1). The underlying
disease in these patients included malignancies (n = 8 [38%]), cholangitis
complicating hepatobiliary calculus (n = 5 [24%]), and urinary tract infection
in debilitated conditions (n = 5 [24%]). In these patients with polymicrobial
infections, the 8 patients with malignancy acquired the infection in the hospital,
whereas the 5 patients with urinary tract infection acquired it in the community.
The antimicrobial susceptibility of the bacteremic isolates of K pneumoniae is shown in Table 3. Community-acquired isolates showed the highest frequency
of resistance to trimethoprim-sulfamethoxazole (n = 22 [23%]), followed by
piperacillin (n = 16 [17%]), cefazolin (n = 13 [14%]), and gentamicin (n =
10 [11%]). Resistance to third-generation cephalosporins was low (<5%).
Among hospital-acquired isolates, resistance to trimethoprim sulfamethoxazole
or piperacillin was most common (n = 28 [44%]), followed by cefazolin (n =
23 [36%]), gentamicin (n = 18 [28%]), cefuroxime (n = 16 [25%]), aztreonam
(n = 16 [25%]), and amikacin (n = 11 [17%]). Resistance to ceftazidime and
ceftriaxone was found in 14 (22%) and 11 patients (17%), respectively. The
resistance of hospital-acquired isolates was significantly higher than that
of the community-acquired isolates (P<.005), except
imipenem. Nosocomial isolates also had a higher overall frequency of resistance
to multiple antibiotics.
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Table 3. Differences of the Antimicrobial Resistance for Klebsiella pneumoniae Bacteremic Isolates From Community-Acquired and
Nosocomial Infections
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SEROTYPING AND CORRELATION AMONG DIFFERENT INFECTIOUS SITES
Of the 158 strains of K pneumoniae, 58 (36.7%)
could be serotyped, and 9 different serotypes were identified (Table 4). The most common were serotypes K1, K2, and K28, and these
accounted for 37 (23.4%), 8 (5.1%), and 6 (3.8%) strains, respectively (Table 4). Typeable isolates were significantly
more common among the community-acquired isolates than among nosocomial isolates
(42/94 [45%] vs 16/64 [25%]; P = .01). Isolation
of the K1 serotype in community-acquired infection was significantly higher
than in nosocomial infection (28/94 [30%] vs 9/64 [14%]; P = .02). On the contrary, nontypeable K pneumoniae was significantly higher in nosocomial infection (48/64 [75%] vs 52/94
[55%]; P = .01; Table 4).
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Table 4. Significant Difference of Capsular Serotype in Bacteremic Klebsiella pneumoniae Isolates Between Community-Acquired
and Nosocomial Infections
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The sources of infection and capsular serotypes of K pneumoniae are shown in Table 5. Most of the bacteremic K pneumoniae isolates
were of a nontypeable serotype when the infection source was the lung, the
urinary tract, or unknown. In contrast, most of the K pneumoniae isolates had an identifiable serotype when the infection source was
in the abdomen. This higher rate of typeable isolates for intra-abdominal
infection compared with other sources of infection was statistically significant
(P = .001). Klebsiella pneumoniae liver abscesses, which were all community acquired, accounted for
23% of the source of community-acquired K pneumoniae
bacteremia. Infection caused by serotypes K1 and K2 was statistically significantly
higher in liver abscess compared with other sources of infection (P = .02). Serotype K1 isolate from unknown infection sources was more
common in the community-acquired infections than in the nosocomial infections
at a statistically significant level (7/15 [47%] vs 4/37 [11%]; P = .02). The presence of serotype K1 isolates, however, was not correlated
with the presence of underlying diabetes mellitus.
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Table 5. Source of Infection and Capsular Serotype of Bacteremic Klebsiella pneumoniae Between Community-Acquired and Nosocomial
Infections
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RISK FACTOR FOR MORTALITY
Nosocomial bacteremia, ceftazidime resistance, leukopenia, and higher
APACHE III scores were identified as risk factors for higher mortality (P<.005; Table 6).
Although no significant difference between community-acquired and nosocomial
bacteremia were observed in lung infection, thrombocytopenia, inappropriate
antibiotic therapy, and septic shock, these variables were all identified
as risk factors associated with significantly higher mortality (P<.05; Table 6).
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Table 6. Significant Risk Factors for Mortality in Patients With Klebsiella pneumoniae Bacteremia*
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COMMENT
Most of the patients in this study were elderly (mean ± SD age,
60 ± 19 years), with a slight male predominance (59%) in the group.
The rate of hospital-acquired K pneumoniae bacteremia
was 40.5%, which was lower than in studies during the past 28 years,1, 6, 17-25
except for a study from Singapore.26
Diabetes mellitus was the most commonly associated condition in patients
with community-acquired K pneumoniae bacteremia,
and the percentage of patients with diabetes (49%) was higher than in previous
studies.1, 6, 17-26
The association of diabetes mellitus and K pneumoniae
liver abscess in Taiwan was reported previously in studies from our institution.27-28 Neoplastic diseases (53%) were the
most commonly associated condition in patients with nosocomial K pneumoniae bacteremia. Longer hospitalization, invasive procedures,
chemotherapy, and the use of antibiotics are common in patients with neoplastic
diseases. A higher rate of fecal colonization by K pneumoniae has been noted in patients with neoplastic diseases than in control
subjects, and this has been associated with antibiotic use.29
Fever occurred at a statistically significant lower rate in patients
with nosocomial bacteremia than those with community-acquired bacteremia (53/64
[83%] vs 88/94 [94%]; P = .03). A higher percentage
of neoplastic diseases, uremia, and corticosteroid use in patients with nosocomial
bacteremia may be responsible. There was a higher percentage of leukopenia
in nosocomial vs community-acquired bacteremia (14/64 [22%] vs 6/94 [6%]; P = .004), and this could have been due to a higher rate
of chemotherapy for neoplastic diseases in the patients with nosocomial bacteremia.
Thrombocytopenia, leukocytosis, shock, and polymicrobial causes were not significantly
different between nosocomial and community-acquired bacteremia.
The nosocomial isolates were significantly more resistant to the antimicrobial
agents that were tested, except for imipenem, when compared with the community-acquired
isolates. More than 20% of the nosocomial strains were resistant to one of
the third-generation cephalosporins, which raises a concern over an increasing
prevalence of extended-spectrum -lactamase (ESBL)–producing K pneumoniae, particularly in hospitals. The ESBL-producing K pneumoniae infections are a risk factor associated with
treatment failure30; therefore, aggressive
infection control, including isolation of patients infected with ESBL-producing K pneumoniae and the imposition of restrictions on the
use of third-generation cephalosporin, should be implemented.
A source of infection was identifiable in 67.1% of cases. The most common
source was a urinary tract infection (20.9%), followed by liver abscess (13.9%).
This finding is similar to those of a study performed in Singapore,25 but has not been reported elsewhere for other Klebsiella bacteremia studies. In our study, of the 22
patients with liver abscess, a metastatic infection developed in 3 (one had
endophthalmitis, a brain abscess, and septic pulmonary emboli; endophthalmitis
developed in another; and the last one had meningitis). Metastatic infection
is a characteristic feature of K pneumoniae liver
abscesses in Taiwan.27, 31-33
Bacteremia with an unknown source of infection was more commonly associated
with nosocomial than with community-acquired infections (58% vs 16%; P<.001). Many patients in whom nosocomial bacteremia
develops have been subjected to invasive procedures such as urinary catheterization
or manipulation, respiratory assistance, central venous catheterization, and
recent surgery, which suggests that the procedure itself may be responsible
for the bacteremia.
The seroepidemiology of Klebsiella infection
has been explored in a number of studies, but none of them have clearly identified
a relationship between the capsular serotype and specific clinical diseases.
The aim of the present study was to correlate the relationship between the
capsular serotype of bacteremic K pneumoniae and
the source of infection. We found that serotypes K1 and K2 were common in
isolates from patients with abdominal infections, such as liver abscesses,
and with community-acquired infections from an unknown source. Klebsiella pneumoniae liver abscess is a well-known disease in Taiwan
that presents as a serious infectious complication in patients with diabetes.28 For nosocomial infections, nontypeable isolates were
predominant when the source of infection was identified as the lung, the urinary
tract, or an unknown source.
Of the 158 strains of K pneumoniae, 58 (36.7%)
could be serotyped, and 9 different serotypes were identified. This differed
from previous reports in which more than 90% of the isolates have been typeable
and the distribution of the serotypes was very wide.9, 13
In Europe and North America, serotypes K2, K21, and K55 (accounting for 8.9%,
7.8% and 4.8%, respectively), made up 21.5% of all isolates, and this was
significantly higher than the remaining serotypes in K pneumoniae bacteremic isolates. In contrast, we found serotypes K1, K2, and K28
accounted for 37 (23.4%), 8 (5.1%), and 6 (3.8%), respectively, of all strains
in this study.
Of the typeable community-acquired bacteremic isolates (n = 42), 34
(81%) were serotypes K1 and K2, especially with an intra-abdominal infection
or an unknown source of infection. Of nosocomial bacteremic isolates, nontypeable
serotypes predominated (48/64 [75%]). Serotypes K1 and K2 have been described
as the predominant typeable serotype in Taiwan.12
Serotypes K1 and K2 showed more virulence than other serotypes in mice.34 However, nontypeable capsular serotypes may possess
an epidemiological advantage compared with other strains, and this may enable
them to colonize and infect hospital patients more easily.35-36
Nontypeable serotypes accounted for most of the bacteremic isolates where
the urinary tract or a lung was identified as an infection source. Serotypes
K1 and K2 were significantly more common in patients in whom the source of
infection was liver abscess (11 of 22) than in those with other sources of
infection (P = .02). For all patients with liver
abscesses who developed complications involving metastatic foci, their disease
was attributable to serotype K1 isolates. Whether a specific bacterial strain
of K pneumoniae is associated with liver abscesses
or whether other factors such as race, environment, or the presence of diabetes
mellitus are involved requires further clarification. The high proportion
of nontypeable strains in the study also requires further investigation.
The overall mortality in our series was 22.8%. The reported mortalities
in Klebsiella bacteremia range from 20% to 62%.1, 6, 17-26
In the present study, risk factors for mortality in patients with K pneumoniae bacteremia included nosocomial infection, lung infection,
thrombocytopenia, leukopenia, infection with ceftazidime-resistant isolates,
inappropriate antimicrobial therapy, and septic shock. In contrast to previous
studies,18, 24 an increase in serum
creatinine or total serum bilirubin level at the onset of bacteremia was not
associated significantly with a higher mortality rate. We could not detect
any statistically significant difference for mortality between any typeable
serotype and the nontypeable serotypes.
CONCLUSIONS
Klebsiella pneumoniae bacteremia is a very
important cause of morbidity and mortality in gram-negative bacteremia in
Taiwan, and this is similar to the situation in most medically well-developed
countries. Urinary tract infection and liver abscess were the most common
infection sources for K pneumoniae bacteremia. Diabetes
mellitus, neoplastic diseases, and hepatobiliary diseases were the most common
underlying conditions. Of all community-acquired and nosocomial isolates,
2% and 22%, respectively, were ceftazidime resistant. Thus, strict control
of the use of third-generation cephalosporins and other antibiotics should
be instituted in the community and in the hospital.37
Only 36.7% of K pneumoniae bacteremia isolates could
be serotyped; of these, 45 (78%) were serotypes K1 and K2. This study shows
a significantly higher prevalence of K1 in bacteremic K
pneumoniae isolate in Taiwan, especially in patients with an infection
source identified as liver abscess, biliary tract infection, or unknown. Of
the nosocomial bacteremic isolates, a nontypeable serotype was predominant
in 48 (75%). Further study on the capsular serotype and the virulence of the K pneumoniae is warranted. The mortality rate remains high,
despite proper antimicrobial treatment and supportive measures. Factors indicating
poor prognosis include the presence of a nosocomial infection, a lung infection,
thrombocytopenia, leukopenia, the presence of a ceftazidime-resistant isolate,
the application of an inappropriate antimicrobial therapy, and septic shock.
AUTHOR INFORMATION
Accepted for publication September 6, 2001.
This study was partly supported by grant TSGH-C88-09 from Tri-Service
General Hospital and a grant from the National Health Research Institute,
Taipei, Taiwan.
We thank Monto Ho, MD, for his critical review of the report.
Corresponding author and reprints: Feng-Yee Chang, MD, PhD, Division
of Infectious Diseases and Tropical Medicine, Tri-Service General Hospital,
No. 325, Section 2, Cheng-Kung Road, Neihu, 114 Taipei, Taiwan (e-mail: fychang{at}ndmctsgh.edu.tw).
From the Division of Infectious Diseases and Tropical Medicine, Department
of Internal Medicine, Tri-Service General Hospital, National Defense Medical
Center (Drs Tsay and Chang), the Division of Clinical Research, National Health
Research Institute (Dr Siu), and the Division of Infectious Diseases, Department
of Medicine, Taipei Veterans General Hospital and National Yang-Ming University
(Dr Fung), Taipei, Taiwan. Dr Tsay is now with the Division of Infectious
Diseases, Department of Internal Medicine, Changhua Christian Hospital, Changhua,
Taiwan.
REFERENCES
| |
1. Yinnon AM, Butnaru A, Raveh D, Jerassy Z, Rudensky B. Klebsiella bacteraemia: community versus nosocomial
infection. QJM. 1996;89:933-941.
ABSTRACT
2. Montgomerie JZ. Epidemiology of Klebsiella and hospital-associated
infections. Rev Infect Dis. 1979;1:736-753.
ISI
| PUBMED
3. Bryan CS, Reynolds KL, Brenner ER. Analysis of 1186 episodes of gram-negative bacteremia in non-university
hospitals: the effects of antimicrobial therapy. Rev Infect Dis. 1983;5:629-638.
ISI
| PUBMED
4. Meyer KS, Urban C, Eagan JA, Berger BJ, Rahal JJ. Nosocomial outbreak of Klebsiella infection
resistant to late-generation cephalosporins. Ann Intern Med. 1993;119:353-358.
FREE FULL TEXT
5. Philippon A, Labia R, Jacoby G. Extended-spectrum -lactamases. Antimicrob Agents Chemother. 1989;33:1131-1136.
FREE FULL TEXT
6. Wang LS, Lee FY, Cheng DL, Liu CY, Hinthorn DR, Jost PM. Klebsiella pneumoniae bacteremia: analysis
of 100 episodes. J Formos Med Assoc. 1990;89:756-763.
PUBMED
7. Domenico P, Johanson WG Jr, Straus DC. Lobar pneumonia in rats produced by clinical isolates of Klebsiella pneumoniae. Infect Immun. 1982;37:327-335.
FREE FULL TEXT
8. Ehrenworth L, Baer H. The pathogenicity of Klebsiella pneumoniae
for mice: the relationship to the quantity and rate of production of type-specific
polysaccharide. J Bacteriol. 1956;72:713-717.
FREE FULL TEXT
9. Martin WJ, Yu PKW, Washington JA. Epidemiological significance of Klebsiella pneumoniae: a 3-month study. Mayo Clin Proc. 1971;46:785-793.
ISI
| PUBMED
10. Selden R, Lee S, Wang WLL, Bennett JV, Eickhoff TC. Nosocomial Klebsiella infections: intestinal
colonization as a reservoir. Ann Intern Med. 1971;74:657-664.
11. Riser E, Noone P. Klebsiella capsular type versus site of isolations. J Clin Pathol. 1981;34:552-555.
FREE FULL TEXT
12. Fung CP, Hu BS, Chang FY, et al. A 5-year study of the seroepidemiology of Klebsiella
pneumoniae: high prevalence of capsular serotype K1 in Taiwan and implication
for vaccine efficacy. J Infect Dis. 2000;181:2075-2079.
FULL TEXT
|
ISI
| PUBMED
13. Cryz SJ Jr, Mortimer PM, Mansfield V, Germanier R. Seroepidemiology of Klebsiella bacteremic
isolates and implications for vaccine development. J Clin Microbiol. 1986;23:687-690.
FREE FULL TEXT
14. National Committee for Clinical Laboratory Standards. Performance Standards for Antimicrobial Disk Susceptibility
Tests: Approved Standard M2-A6. Villanova, Pa: National Committee for Clinical Laboratory Standards;
1997.
15. Palfreyman JM. Klebsiella serotyping by counter-current immunoelectrophoresis. J Hyg (Lond). 1978;81:219-225.
16. Knaus WA, Wagner DP, Draper EA, et al. The APACHE III prognostic system: risk prediction of hospital mortality
for critically ill hospitalized adults. Chest. 1991;100:1619-1636.
FREE FULL TEXT
17. Korvick JA, Bryan CS, Farber B, et al. Prospective observational study of Klebsiella
bacteremia in 230 patients: outcome for antibiotic combinations versus monotherapy. Antimicrob Agents Chemother. 1992;36:2639-2644.
FREE FULL TEXT
18. Watanakunakorn C, Jura J. Klebsiella bacteremia: a review of 196 episodes
during a decade (1980-1989). Scand J Infect Dis. 1991;23:399-405.
ISI
| PUBMED
19. Garcia de la Torres M, Romero-Vivas J, Martinez-Beltran J, Guerrero A, Meseguer M, Bouza E. Klebsiella bacteremia: an analysis of 100
episodes. Rev Infect Dis. 1985;7:143-150.
ISI
| PUBMED
20. Bodey GP, Elting LS, Rodriquez S, Hernandez M. Klebsiella bacteremia: A 10-year review in
a cancer institution. Cancer. 1989;64:2368-2376.
FULL TEXT
|
ISI
| PUBMED
21. Haddy RI, Lee III L, Sangal SP, Walbroehl GS, Hambrick CS, Santi GM. Klebsiella pneumoniae bacteremia in the community
hospital. J Fam Pract. 1989;28:686-690.
ISI
| PUBMED
22. Montgomerie JZ, Ota JK. Klebsiella bacteremia. Arch Intern Med. 1980;140:525-527.
ABSTRACT
23. Bonadio WA. Klebsiella pneumoniae bacteremia in children:
fifty-seven cases in 10 years. AJDC. 1989;143:1061-1063.
24. Feldman C, Smith C, Levy H, Ginsburg P, Miller SD, Koornhof HJ. Klebsiella pneumoniae bacteremia at an urban
general hospital. J Infect. 1990;20:21-31.
FULL TEXT
|
ISI
| PUBMED
25. Umsawasdi T, Middleman EA, Luna M, Bodey GP. Klebsiella bacteremia in cancer patients. Am J Med Sci. 1973;265:473-482.
ISI
| PUBMED
26. Lee KH, Hui KP, Tan WC, Lim TK. Klebsiella bacteremia: a report of 101 cases
from National University Hospital, Singapore. J Hosp Infect. 1994;27:299-305.
FULL TEXT
|
ISI
| PUBMED
27. Chang FY, Chou MY. Comparison of pyogenic liver abscesses caused by Klebsiella pneumoniae and non–K pneumoniae pathogens. J Formos Med Assoc. 1995;94:232-237.
PUBMED
28. Chang FY, Chou MY, Fan RL, Shaio MF. A clinical study of Klebsiella liver abscess. Taiwan Yi Xue Hui Za Zhi. 1988;87:282-287.
PUBMED
29. Rose HD, Schrerer J. The effect of hospitalization and antibiotic therapy on the gram-negative
fecal flora. Am J Med Sci. 1968;225:228-236.
30. Schiappa DA, Hayden MK, Matushek MG, et al. Ceftazidime-resistant Klebsiella pneumoniae
and Escherichea coli bloodstream infection: a case-control
and molecular epidemiologic investigation. J Infect Dis. 1996;174:529-536.
ISI
| PUBMED
31. Wang JH, Liu YC, Lee SS, et al. Primary liver abscess due to Klebsiella pneumoniae in Taiwan. Clin Infect Dis. 1998;26:1434-1438.
ISI
| PUBMED
32. Liu YC, Cheng DL, Lin CL. Klebsiella pneumoniae liver abscess associated
with septic endophthalmitis. Arch Intern Med. 1986;146:1913-1916.
ABSTRACT
33. Cheng DL, Liu YC, Yen MY, Liu CY, Wang RS. Septic metastatic lesions of pyogenic liver abscess. Arch Intern Med. 1991;151:1557-1559.
ABSTRACT
34. Mizuta K, Ohta M, Mori M, Hasegawa T, Nakashima I, Kato N. Virulence for mice of Klebsiella strains belonging
to O1 group: relationship to their capsular (K) types. Infect Immun. 1983;40:56-61.
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