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Pyogenic Liver Abscesses Caused by Klebsiella pneumoniae: US Appearance and Aspiration Findings¹

¹ From the Department of Diagnostic Radiology and Organ Imaging, United Christian Hospital (J.Y.H.H., M.K.W.Y., D.H.Y.C., A.L., T.K.L.L., J.C.S.C.), 130 Hip Wo Street, Kwun Tong, Hong Kong; and Department of Microbiology, the University of Hong Kong, Queen Mary Hospital, Hong Kong (P.C.Y.W.). Received August 12, 2005; revision requested October 17; revision received December 18; accepted January 5, 2006; final version accepted July 25. Address correspondence to J.Y.H.H. (e-mail: jhuiyh{at}yahoo.com.hk).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE References

 
Purpose: To retrospectively compare the ultrasonographic (US) appearance and amount of pus obtained at initial aspiration for liver abscesses caused by Klebsiella pneumoniae with those for liver abscesses caused by other bacterial pathogens.

Materials and Methods: This study had medical ethics committee approval; informed consent was not required. Asian patients with pyogenic liver abscesses in a 5-year period were included. Abscess clinical, laboratory, and microbiologic characteristics and treatment and outcome were analyzed. US images were classified according to the size of the largest liver abscess, the echogenic pattern of the lesion, the presence of any echogenic debris within the lesion, increased through transmission in the posterior aspect of the lesion, and the lesion margin. Clinical and US characteristics of patients with K pneumoniae monomicrobial liver abscesses and those with non–K pneumoniae monomicrobial or polymicrobial liver abscesses were compared. The ² or Fisher exact test was used for categorical variables; the Student t test was used for continuous variables.

Results: There were 120 patients with pyogenic liver abscesses. Median patient age was 69 years (range, 13–94 years). Fifty-nine patients were male, and 61 were female. Fifty patients with K pneumoniae monomicrobial and 33 patients with non–K pneumoniae monomicrobial or polymicrobial liver abscesses underwent US. K pneumoniae monomicrobial liver abscesses were associated with diabetes mellitus (P < .001), higher blood glucose levels at admission (P < .05), predominantly solid US appearances (P < .001), irregular or indistinct lesion margins (P < .05), less than 2 mL of pus aspirated (P < .001), and longer duration of antibiotic treatment (P < .05).

Conclusion: A predominantly solid appearance at US is associated with K pneumoniae monomicrobial liver abscess. K pneumoniae liver abscess is associated with a much smaller quantity of pus at initial aspiration.

Supplemental material: http://radiology.rsnajnls.org/cgi/content/full/242/3/769/DC1

© RSNA, 2007

	INTRODUCTION

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The accurate diagnosis of pyogenic liver abscesses with ultrasonography (US) may be difficult because of their varied and time- and histologic nature–dependent appearances (1,2) and the resemblance of the US features of liver abscesses to those of other liver diseases (1–3). US appearances of liver abscesses may range from cystic to highly echogenic. This variation has a close relationship to the pathologic stage of the liver abscess (1,3). During the early stage of abscess formation before the hepatocytes undergo necrosis, a pyogenic liver abscess appears solid (1,4). At this stage, lesions may be easily confused with other intrahepatic diseases, particularly primary or secondary liver tumors (2–5). When the liver abscess starts to liquefy, it will appear increasingly fluid with mixed echogenicity at US (1,4). At a later stage, when the abscess matures with central liquefaction, it will appear as a predominantly cystic lesion (1,4). Histologically, at this stage, most pyogenic liver abscesses appear as multiloculated cystic lesions, with the locules communicating freely with each other (6,7). Because this is also the stage in which most patients with pyogenic liver abscesses present clinically, classically, most pyogenic liver abscesses are cystic at US, and percutaneous aspiration (with or without drainage catheter insertion) together with intravenous antibiotics is recommended as the standard treatment of choice (8,9).

Traditionally, bacterial pathogens commonly associated with pyogenic liver abscesses include flora of the gastrointestinal tract, such as Escherichia coli and other members of the Enterobacteriaceae family, Streptococcus milleri, and Enterococcus species, and anaerobes such as Bacteroides and Clostridium species. In the past 25 years, results of multiple studies have revealed that Klebsiella pneumoniae has been emerging as the most important cause of pyogenic liver abscesses in the Asian population (10). In Western countries, K pneumoniae accounted for about a quarter of all cases of pyogenic liver abscesses (11). In the Chinese population, it has been observed that a disproportionately high incidence of pyogenic liver abscesses and other pus-forming lesions, such as endophthalmitis and pyomyositis, is associated with K pneumoniae (12–14). In one study (10), the percentage of pyogenic liver abscesses caused by K pneumoniae was up to 88%. Furthermore, these K pneumoniae infections in the Chinese population have also been strongly associated with diabetes mellitus (8). Histologically, K pneumoniae liver abscesses consist of aggregates of multiple small locules that do not communicate (15). Only a small amount of pus can be drained in such lesions, and some patients have to undergo hepatectomy as the definitive therapy when the condition fails to resolve with antibiotic treatment and percutaneous drainage (15).

These peculiar histologic findings should affect the US features, and possibly the treatment, of K pneumoniae liver abscesses. However, to our knowledge, there is no report on the comparison of the US appearance of pyogenic liver abscesses caused by K pneumoniae with that of abscesses caused by other bacteria. Thus, the purpose of our study was to retrospectively compare the US appearance and amount of pus obtained at initial aspiration for liver abscesses caused by K pneumoniae with those for liver abscesses caused by other bacterial pathogens.

	MATERIALS AND METHODS

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Patients
The medical ethics committee of our hospital approved the protocol for this retrospective study, which was performed at one institution. Informed consent for reviews of patient records and images was not required. Hospital records of patients discharged with a diagnosis of liver abscess between July 1997 and June 2002 were retrieved. The records were reviewed by one author (D.H.Y.C.) independently, and all patients with lesions that fit the definition of pyogenic liver abscess were included in the study. A pyogenic liver abscess was defined as a hepatic lesion demonstrated at US and/or computed tomography (CT) in a patient with (a) a compatible clinical picture (various combinations of features of sepsis, right upper quadrant pain, and abnormal liver function), (b) one or more of the following: a positive blood culture result, a positive culture result from aspiration of the lesion, and/or a clinical response to antibiotic treatment; and (c) complete resolution of the lesion at follow-up imaging performed up to 6 months after discharge or at autopsy.

Collected Data
Information recorded included patient age, sex, underlying disease(s) (diabetes mellitus, biliary tract disease, chronic renal failure, malignancy, cirrhosis), and body temperature at admission, as documented in the medical history. Initial laboratory values obtained included total and differential white blood cell count, erythrocyte sedimentation rate, and serum blood glucose level. Initial values were the first values obtained within the first 24 hours after presentation. The microbiologic cause(s) of a liver abscess were defined as the organism(s) recovered from the liver abscess and/or blood culture. A monomicrobial liver abscess is one in which only one organism, and no other organism, is recovered from the liver abscess and/or blood culture. A polymicrobial liver abscess is one in which more than one organism (one of which could be K pneumoniae) is recovered from the liver abscess and/or blood culture. The occurrence of any septic metastatic complications in other parts of the body (lung, urinary tract, brain, muscle, eye, and appendix) (10,12) that were caused by the same organism was also recorded. The day on which the US examination was performed with respect to the day of the onset of symptoms and the number of liver abscesses were noted from the radiology report.

Treatment
All patients received antibiotic therapy (most commonly metronidazole and ceftriaxone or amoxicillin/clavulanate) for their abscesses. Treatment also included invasive procedures, such as US- or CT-guided aspiration and/or drainage or open surgery. All image-guided aspiration and/or drainage procedures included in this study were performed by one of seven radiologists, including three authors (J.Y.H.H., with 3 years of experience in US or CT-guided liver abscess aspiration and/or drainage; T.K.L.L., with 10 years of experience; and J.C.S.C., with 13 years of experience); the other radiologists had 5–12 years of experience. In our department, all image-guided aspirations were performed in the same setting or within the same day of the imaging examination by using 15-cm, 18-gauge disposable trocar needles (Cook, Bloomington, Ind). With US or CT guidance, the needle tip was directed into the largest locule within the abscess. A sample of pus was routinely obtained and sent for microbiologic analysis, including Gram staining, bacterial culturing, and antibiotic susceptibility testing.

In general, for abscesses that were larger than 3 cm in diameter and were predominantly cystic at US, drainage catheters would be inserted. If a drainage catheter was inserted, a 0.038-inch extra-stiff guidewire (Amplatz; Cook) would then be introduced into the abscess cavity. After serial dilatations, an 8-F multisidehole pigtail catheter (Angiomed, Karlsruhe, Germany) was inserted into the largest cavity of the abscess and was secured to the skin for continuous external drainage. If a drainage catheter was not inserted, follow-up US or CT with or without aspiration and drainage would be performed if the patient's condition did not improve with antibiotic therapy. The amount of pus obtained at initial aspiration was noted from the radiology report. The duration of antibiotic therapy, duration of hospital stay, and final outcomes of the patients were also determined.

Retrospective Classification of US Pattern for Liver Abscesses
US was performed with two real-time scanners: One unit (HDI 3000; Advanced Technology Laboratories, Bothell, Wash) that was equipped with a multifrequency (5.0–2.0-MHz) curved linear array probe and a second unit (Sequoia 512; Acuson, Mountain View, Calif) that was equipped with a multifrequency (4.0–2.0-MHz) vector array transducer. During the retrospective analysis, hard-copy US images were independently evaluated by two radiologists (T.K.L.L. and J.Y.H.H.) who were blinded to the patient's name, cause of the liver abscess, and all other clinical characteristics of the patients. Both reviewers were experienced in hepatic US (with 15 and 9 years of experience in US imaging, respectively) and in most studies; they had performed the original US examinations and interpreted the findings. US images were reviewed to determine the size of the largest lesion as documented with electronic calipers. The observers categorized the predominant pattern on the US images. The final classification represented concordant independent judgments. When the two reviewers expressed discordant opinions, consensus decisions were made with a joint review of the recorded images.

On the basis of findings at the retrospective analysis by the reviewers, the US pattern of the largest liver abscess in each patient was classified as follows: (a) a predominantly cystic or liquefied lesion, with a cystic component occurring in greater than 50% of the abscess; (b) a predominantly solid or tumorlike lesion, characterized by the presence of a cystic component in less than 50% of the lesion; or (c) a gas-containing lesion, represented by the presence of high-signal-intensity internal echoes with posterior reverberation artifacts and back shadowing that obscured much of the internal structure. Except for patients with gas-containing lesions, we noted the presence of any echogenic debris within the lesion or increased through transmission in the posterior aspect of the lesion, as well as the margins of the lesion (smooth, irregular, or indistinct).

Statistical Analysis
Statistical analyses were performed with a software package (SPSS 11.0; SPSS, Chicago, Ill). Patients who did not undergo US were excluded from the statistical analysis. A comparison of characteristics between patients with K pneumoniae monomicrobial liver abscesses and patients with non–K pneumoniae monomicrobial or polymicrobial pyogenic liver abscesses was performed. The ² or Fisher exact test was used for categorical variables, and the Student t test was used for continuous variables, with or without Bonferroni correction. P < .05 was regarded as indicating a statistically significant difference.

	RESULTS

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Patients
During the 5-year period, a total of 120 patients had lesions that fit the definition of a pyogenic liver abscess (Table 1). The median age of the patients was 69 years (range, 13–94 years). Fifty-nine patients were male, and 61 were female. Forty-four (37%) patients had diabetes mellitus, 44 (37%) had a history of biliary tract disease, 16 (13%) had chronic renal failure, 15 (12%) had malignancy, and eight (7%) had liver cirrhosis. Their mean temperature at admission was 38.5°C, with a mean white cell count of 17.5 x 10⁹/L, a mean neutrophil count of 15.9 x 10⁹/L, a mean lymphocyte count of 1.0 x 10⁹/L, a mean erythrocyte sedimentation rate of 90.5 mm/h, and a mean blood glucose level of 9.9 mmol/L. Ninety-six (80%) patients had positive blood and/or abscess aspirate cultures; 69 (58%) patients had monomicrobial and 27 (22%) patients had polymicrobial liver abscesses. The five most common organisms recovered were K pneumoniae (n = 61 [51%]), E coli (n = 22 [18%]), S milleri (n = 13 [11%]), Enterobacter species (n = 12 [10%]), and Bacteroides species (n = 10 [8%]). Fifty-one (42%) patients had positive blood cultures. Seventeen (14%) patients had concomitant foci of infection in other parts of the body: Twelve (10%) had lung abscesses, three (2%) had urinary tract infections, two (2%) had brain abscesses, two (2%) had pyomyositis, one (1%) had endophthalmitis, and one (1%) had an appendicular abscess.

K pneumoniae Abscess
The characteristics of the 61 patients with K pneumoniae pyogenic liver abscesses (Table E1, http://radiology.rsnajnls.org/cgi/content/full/242/3/769/DC1) indicated that the male-to-female ratio was 30:31. The median age of these patients was 70 years (range, 13–91 years). Thirty-two (52%) patients had diabetes mellitus, 18 (30%) had a history of biliary tract disease, seven (11%) had chronic renal failure, three (5%) had malignancy, and three (5%) had liver cirrhosis. Patients with K pneumoniae pyogenic liver abscesses underwent US a median of 5 days after the onset of symptoms (mean, 6.1 days ± 4.2 [standard deviation]). The US appearance of the abscesses in 51 (84%) patients was predominantly solid (Figs 1, 2), while that in six (10%) patients was predominantly cystic (Fig 3). None of the K pneumoniae pyogenic liver abscesses appeared to be gas-containing lesions (Fig 4) at US in our study. US was not performed in four (7%) patients. Fourteen (23%) patients had concomitant foci of infection in other parts of the body: Ten (16%) patients had lung abscesses, three (5%) patients had urinary tract infections, two (3%) patients had brain abscesses, two (3%) patients had pyomyositis, and one (2%) patient had endophthalmitis. Fifty-four (89%) patients had monomicrobial K pneumoniae pyogenic liver abscesses; in the remaining seven (11%) patients, other organisms in addition to K pneumoniae were recovered from blood and/or abscess aspirate cultures. Overall, nine (15%) of the 61 patients died.

View larger version (93K): [in this window] [in a new window] [Download PPT slide]   Figure 1a: (a) Transverse and (b) oblique US images in 64-year-old woman (patient 38 in Table E1, http://radiology.rsnajnls.org/cgi/content/full/242/3/769/DC1) with K pneumoniae liver abscess (between crosshairs) in right hepatic lobe. Central cystic component (arrowheads) occurs in less than half of the lesion, giving it a predominantly solid appearance. This lesion has a smooth margin (arrow).

View larger version (135K): [in this window] [in a new window] [Download PPT slide]   Figure 1b: (a) Transverse and (b) oblique US images in 64-year-old woman (patient 38 in Table E1, http://radiology.rsnajnls.org/cgi/content/full/242/3/769/DC1) with K pneumoniae liver abscess (between crosshairs) in right hepatic lobe. Central cystic component (arrowheads) occurs in less than half of the lesion, giving it a predominantly solid appearance. This lesion has a smooth margin (arrow).

View larger version (165K): [in this window] [in a new window] [Download PPT slide]   Figure 2: Transverse US image of left lobe of liver in 53-year-old man (patient 17 in Table E1, http://radiology.rsnajnls.org/cgi/content/full/242/3/769/DC1) shows predominantly solid K pneumoniae liver abscess (arrow) with a cystic component occurring in less than half of the lesion. The lesion is bulging on the liver capsule and is poorly marginated. There is no increase in through transmission.

View larger version (126K): [in this window] [in a new window] [Download PPT slide]   Figure 3: Transverse US image of right lobe of liver in 62-year-old man with a well-liquefied, predominantly cystic liver abscess (arrow) caused by multiple organisms other than K pneumoniae. The lesion margin is irregular, and there is increased through transmission posteriorly. No definite echogenic debris is seen inside the lesion.

View larger version (118K): [in this window] [in a new window] [Download PPT slide]   Figure 4: Oblique US image of right hepatic lobe in 54-year-old man shows gas-containing liver abscess (between crosshairs) caused by E coli. Back shadowing obscures the deeper part of the lesion.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE References

K pneumoniae liver abscess is associated with a relatively small quantity of pus at initial aspiration. Our current standard treatment for pyogenic liver abscesses greater than 3 cm in diameter is antibiotics and percutaneous drainage or repeated aspiration. In our study, for polymicrobial or non–K pneumoniae monomicrobial pyogenic liver abscesses, initial aspiration yielded more than 10 mL of pus in more than 80% of patients. On the other hand, for monomicrobial K pneumoniae liver abscesses, initial aspiration yielded less than 10 mL of pus in all patients and less than 2 mL of pus in more than 80%. This poor yield at aspiration is probably related to the association of K pneumoniae liver abscesses with the aggregation of multiple small locules that do not communicate, meaning that such abscesses possibly represent an immature form of liver abscess with failure of liquefaction (15).

Recently, it has been noted that a diameter of greater than 5 cm; concomitant sepsis; intrahepatic gas formation; an Acute Physiology and Chronic Health Evaluation III, or APACHE III, score of greater than 40; and delayed or inadequate drainage are important determinants of poor prognosis in K pneumoniae pyogenic liver abscess (16). Furthermore, diabetes mellitus, large abscess size, gas formation in the liver abscess, and left lobe involvement are risk factors for spontaneous rupture in patients with K pneumoniae liver abscess (17). We believe further prospective studies are needed to determine the best treatment strategy for patients with K pneumoniae liver abscess.

The association of K pneumoniae liver abscesses with such a predominantly solid appearance at US is probably related to their failure of liquefaction. It has been observed that pyogenic liver abscesses in the Chinese population with diabetes mellitus are often associated with K pneumoniae (10,14). It has also been shown that both a high degree of genetic similarity is present in more than 60% of the K pneumoniae strains (18) and a high prevalence of phagocytosis-resistant capsular serotype is present in the K pneumoniae strains associated with these liver abscesses (19). Recently, a virulence gene, magA, which encodes a 43-kDa outer membrane protein, was shown to be more prevalent in invasive strains of K pneumoniae that cause primary liver abscesses and septic metastatic complications (20). The wild-type magA K pneumoniae strains produced a mucoviscous polysaccharide web, actively proliferated in nonimmune human serum, resisted phagocytosis, and caused liver microabscess and meningitis in mice. However, magA^– mutants without the exopolysaccharide web became extremely serum sensitive and phagocytosis susceptible and were avirulent to mice. Therefore, it is very likely that, in a diabetic patient predisposed to have impaired phagocytosis functions (21–24), these magA⁺ K pneumoniae strains with this additional virulence factor would render the abscesses extremely difficult to phagocytose. This poor phagocytosis would hamper the killing of the K pneumoniae microbe and, hence, liquefaction of the abscess.

Regarding the outcome of our patients, the overall mortality rate in our series (18%) is concordant with previously reported rates (5.2%–41.0%) (9,25–30). In some studies (9,30), K pneumoniae liver abscess was reported to confer a lower mortality, whereas in the present series, both patients with K pneumoniae and patients with non–K pneumoniae liver abscesses had similar mortality rates. Further studies on both the K pneumoniae strains and the host susceptibility in various populations would be required to elucidate the different mortality rates in different populations.

Our study had limitations. First, the criteria for diagnosis were not applied prospectively. A prospective study of this predominantly solid or predominantly cystic pattern-based classification is needed to confirm its usefulness in the diagnosis of liver abscesses caused by K pneumoniae. Second, the proportion of liver abscesses caused by K pneumoniae in our study population appears to be relatively high compared with that in Western countries. Third, we did not include an evaluation of interobserver agreement in the classification of liver abscesses. However, we believe that the classification is simple and is easy to apply. Fourth, only 69% of patients with pyogenic liver abscesses with known causative organisms underwent US. The other patients were evaluated with CT only. This probably was a result of individual clinicians' preferences and would not lead to any bias in the results.

In conclusion, unlike the classic cystic liver abscesses caused by other pyogenic organisms, K pneumoniae liver abscesses tend to be less liquefied, with a predominantly solid appearance at US, and are associated with a small quantity of pus obtained at initial aspiration.

	ADVANCES IN KNOWLEDGE

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• Klebsiella pneumoniae monomicrobial liver abscess, when compared with non–K pneumoniae monomicrobial or polymicrobial liver abscess, is associated with a predominantly solid appearance, no increased through transmission in the posterior aspect of the lesion, and an irregular or indistinct lesion margin at US.
  
• K pneumoniae monomicrobial liver abscess, when compared with non–K pneumoniae monomicrobial or polymicrobial liver abscess, is associated with a relatively small quantity of pus obtained at initial aspiration.
  

	FOOTNOTES

 
Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, J.Y.H.H., M.K.W.Y., D.H.Y.C., P.C.Y.W.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, J.Y.H.H., M.K.W.Y., D.H.Y.C., P.C.Y.W.; clinical studies, J.Y.H.H., M.K.W.Y., D.H.Y.C., A.L., T.K.L.L.; statistical analysis, J.Y.H.H., M.K.W.Y., P.C.Y.W.; and manuscript editing, J.Y.H.H., M.K.W.Y., T.K.L.L., J.C.S.C., P.C.Y.W.

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