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J Clin Microbiol. Feb 2007; 45(2): 466–471.
Published online Dec 6, 2006. doi:  10.1128/JCM.01150-06
PMCID: PMC1829066

Capsular Serotype K1 or K2, Rather than magA and rmpA, Is a Major Virulence Determinant for Klebsiella pneumoniae Liver Abscess in Singapore and Taiwan[down-pointing small open triangle]

Abstract

Capsular serotypes, magA, and rmpA have been documented in high prevalence for Klebsiella pneumoniae liver abscess. To investigate the regional difference and the correlation of capsular serotype, magA, and rmpA with virulence, 73 isolates were collected in Singapore and Taiwan. Capsular serotypes were determined by countercurrent immunoelectrophoresis, the presence of magA and rmpA was determined by PCR, and virulence was determined by phagocytosis and mouse inoculation. Isolates from Singapore were similar to those from Taiwan in genomic heterogeneity, prevalence of serotype, and the presence of magA and rmpA. The most common serotype was K1 (34/73; 46.6%), followed by K2 (15/73; 20.5%). magA was restricted to serotype K1. All K1 or K2 isolates and 66.7% (16/24) of isolates that were neither serotype K1 nor serotype K2 (non-K1/K2) carried rmpA. Serotype K1 or K2 isolates demonstrated significantly more phagocytic resistance and virulence than did rmpA-positive and -negative groups of non-K1/K2 isolates. In the non-K1/K2 group, the virulence profiles of rmpA-positive strains from Taiwan and Singapore were different by phagocytosis assay and in the mouse model, indicating that factors other than rmpA contributed to virulence. The characteristics of K. pneumoniae liver abscess in Singapore and Taiwan are similar. Capsular serotype K1 or K2 plays a more important role than magA and rmpA in determining virulence in K. pneumoniae liver abscess.

Klebsiella pneumoniae is a common gram-negative pathogen causing both community and nosocomial infections (17). In the past two decades, a new type of invasive K. pneumoniae disease has emerged in Taiwan that typically presents as a community-acquired primary liver abscess (12, 23). Several reports, especially from the Asia Pacific region and the United States, have observed that this pathogen has become the predominant cause of liver abscess instead of the previously described amoebae, Escherichia coli, streptococci, and anaerobic bacteria (9, 15, 25). Metastatic septic meningitis and endophthalmitis are severe complications of K. pneumoniae liver abscess.

Several studies of bacterial pathogenesis in Taiwan have documented that serotype K1 or K2, magA, and rmpA are possible virulence factors in K. pneumoniae liver abscess. In our previous study, 77.6% of K. pneumoniae liver abscesses were caused by serotype K1 or K2 isolates (6). Serotype K1 or K2 isolates were significantly more prevalent in strains causing liver abscess than in the strains causing bacteremia alone (22). magA has been reported in 98.1% and 83.3% of K. pneumoniae strains isolated from patients with liver abscess and was significantly more prevalent than the bacteremic strains (4, 5). Furthermore, the presence of rmpA in 87.5% of liver abscess strains was also documented by another group and the prevalence was significantly higher than that in bacteremic strains as well (26). However, the correlations of these virulence factors and their contribution to virulence have not been well compared.

Since all of the above studies collected isolates from the same locality, whether these factors reflected local variation remained to be clarified. In the present study, we have tried to use isolates collected in Singapore and Taiwan in the same period of time to delineate the correlation of capsular serotype, magA, and rmpA with virulence as well as regional variation.

MATERIALS AND METHODS

Case definition and bacterial isolates.

K. pneumoniae strains isolated from patients with liver abscesses were collected at Singapore General Hospital in Singapore and Tri-Service General Hospital in Taiwan from 2002 to 2004. Consecutive patients with K. pneumoniae liver abscess were enrolled in the study if computed tomographic scanning revealed one or more space-occupying lesions or ultrasonography showed one or more areas of echolucency in the liver and a culture of computed tomographic-guided or ultrasound-guided percutaneous liver aspirates and/or blood revealed K. pneumoniae. The identification of the isolates was performed according to standard clinical microbiologic methods. Among the 73 strains isolated from patients with liver abscesses, 40 strains were obtained from Singapore and 33 were from Taiwan. All strains were stored at −80°C before use.

Capsular serotyping.

All isolates were serotyped by a countercurrent immunoelectrophoresis method (16). Antisera were kindly provided by the Laboratory of Hospital Infection, Central Public Health Laboratory, presently named the Health Protection Agency, London, United Kingdom. Control K. pneumoniae serotypes, which were acquired from the American Type Culture Collection (ATCC, Rockville, MD), included ATCC 4208 (serotype K1), ATCC 13883 (serotype K3), and ATCC 700603 (serotype K6).

PFGE.

Total DNA was prepared, and pulsed-field gel electrophoresis (PFGE) was performed as described previously (18). The restriction enzyme XbaI (New England Biolabs, Beverly, MA) was used. Restriction fragments were separated by PFGE in 1% agarose gels (Bio-Rad, Hercules, CA) in 0.5× Tris-boric acid-EDTA buffer using a Bio-Rad CHEF-Mapper apparatus (Bio-Rad Laboratories, Richmond, CA). Gels were stained with ethidium bromide and photographed under UV light. Band patterns were visually compared and classified according to previously described criteria (21) as indistinguishable (clonal), closely related (clonal variants [at least three band differences]), possibly related (four to six band differences), and unrelated (more than six band differences).

PCR.

PCR was used to determine the prevalence of magA and rmpA. An overnight-cultured bacterial colony was added to 300 μl water and boiled for 15 min to release DNA template. Previously published primers used for PCR were, for magA forward, 5′-GGTGCTCTTTACATCATTGC-3′ and, for magA reverse, 5′-GCAATGGCCATTTGCGTTAG-3′ (4, 5), and for rmpA forward, 5′-ACTGGGCTACCTCTGCTTCA-3′, and for rmpA reverse, 5′-CTTGCATGAGCCATCTTTCA-3′ (26). The chromosomal blaSHV-1a gene was used as an internal positive control with primers designed as forward, 5′-ATCTGGTGGACTACTCGC-3′, and reverse, 5′-GCCTCATTCAGTTCCGTT-3′. The reaction mixture was kept at 95°C for 5 min, followed by 40 temperature cycles of 95°C for 1 min, 50°C for 1 min, and 72°C for 2 min, and 72°C for 7 min. The expected PCR products of magA, rmpA, and the positive internal control were 1,282, 535, and 213 bp in length, respectively.

Phagocytosis assay.

The neutrophil isolation from healthy volunteers and the bacterial labeling with fluorescein isothiocyanate (FITC) were performed as previously described (7, 11). The mixture of the labeled bacteria, the neutrophil suspension, the pooled normal human serum, and the phosphate-buffered saline (PBS; pH 7.4) was incubated for 0 and 10 min in a shaking 37°C water bath. By removal of the supernatant after centrifugation, the cell pellet was resuspended in the ice-cold PBS solution and the ethidium bromide solution was added. FITC fluorescence was detected by using FACScan (Becton Dickinson Immunocytometry Systems, San Jose, CA). By using the logarithmic amplifier, we displayed fluorescence distribution data as single histograms for FL1-H. The percentage of the neutrophils which carried FITC-stained bacteria at 10 min was adjusted with the percentage at 0 min, and the adjusted percentage was used as the phagocytosis rate.

Mouse inoculation.

Male 6-week-old BALB/c mice were used for inoculation. A standard inoculum of 2 × 104 to 6 × 104 CFU of K. pneumoniae in the mid-logarithmic phase of growth was diluted in 100 μl PBS and injected intraperitoneally. Six mice were used to test the effects of each strain. The mice were observed for 2 weeks after inoculation. The animal experiments were approved by the Institutional Review Board of Tri-Service General Hospital, Taiwan.

Statistical analysis.

Student's t test was used for statistical analysis. Data were expressed as means ± standard deviations (SD). P values of less than 0.05 were considered statistically significant.

RESULTS

Serotype prevalence.

All of the 73 isolates were serotyped, and 64 (87.7%) isolates were typeable. A total of 14 of the 77 known capsular serotypes were identified. There was no significant difference in the prevalence of each serotype between isolates from Singapore and Taiwan (Table (Table1).1). Serotypes K1 and K2 were predominant, accounting for 46.6% (34/73) and 20.5% (15/73) of all isolates, respectively. Serotype K1 isolates occurred at a significantly higher frequency than all other serotypes (P < 0.001). Serotype K1 or K2 isolates were significantly more prevalent than those that were neither K1 nor K2 (non-K1/K2) (49/73 versus 24/73; P < 0.001).

TABLE 1.
Serotype prevalence of Klebsiella pneumoniae isolates causing liver abscesses in Singapore and Taiwan between 2002 and 2004

PFGE.

PFGE was performed on 34 isolates of serotype K1 (16 from Singapore and 18 from Taiwan) (Fig. 1A and B) and 15 isolates of serotype K2 (8 from Singapore and 7 from Taiwan) (Fig. 1C and D). Three pairs of serotype K1 strains had indistinguishable PFGE patterns, one from Singapore and two from Taiwan. According to previously described criteria, there was no major cluster of isolates found among those isolates with the same serotype from the same region. A high degree of genetic polymorphism was observed in both groups from Singapore and Taiwan.

FIG. 1.
Dendrogram of PFGE patterns for 49 isolates of serotype K1 or K2 Klebsiella pneumoniae causing liver abscess.

Prevalence of magA and rmpA in isolates with different serotypes.

To investigate the prevalence of magA and rmpA and their association with capsular serotype, all of the 73 isolates were classified into three groups (serotype K1, serotype K2, and non-K1/K2) and screened by PCR. In each group, there was no significant difference in the prevalence of magA and rmpA between strains from Singapore and Taiwan (Table (Table22).

TABLE 2.
Prevalence of magA and rmpA genes in relation to serotype in Klebsiella pneumoniae isolates causing liver abscesses in Singapore and Taiwan between 2002 and 2004

magA was present in all 34 isolates serotyped as K1 and absent in all 39 strains of serotypes other than K1. Sixty-five (89.0%) of all 73 isolates were positive for rmpA. All 34 isolates of serotype K1, all 15 isolates of serotype K2, and 16 (66.7%) out of 24 non-K1/K2 isolates carried rmpA. rmpA was significantly more prevalent in serotype K1 or K2 than in non-K1/K2 isolates (49/49 versus 16/24; P < 0.001).

Phagocytosis assay and mouse lethality.

To further investigate the correlation of capsular serotype, magA, and rmpA with phagocytosis resistance, all 73 isolates were assayed and classified. Since magA was unique to serotype K1 strains and all of the serotype K1 and K2 strains were rmpA positive, we classified all strains into four groups: serotype K1 (magA positive and rmpA positive), serotype K2 (magA negative and rmpA positive), rmpA-positive non-K1/K2 (magA negative), and rmpA-negative non-K1/K2 (magA negative).

In each group, there was no significant difference in phagocytosis rate between strains from Singapore and Taiwan (P was 0.15, 0.17, 0.18, and 0.19 for serotypes K1 and K2 and rmpA-positive and rmpA-negative non-K1/K2 groups, respectively) (Fig. (Fig.2).2). Overall, there was no significant difference for phagocytosis between the serotype K1 and K2 groups (P = 0.052). Among the non-K1/K2 strains, the rmpA-positive group was significantly more resistant to phagocytosis than was the rmpA-negative group (P < 0.01). Both of the serotype K1 and K2 groups were significantly more resistant to phagocytosis than both of the rmpA-positive and rmpA-negative non-K1/K2 groups (P < 0.01). Serotype K1 or K2 strains were significantly more phagocytosis resistant than the non-K1/K2 strains (P < 0.01).

FIG. 2.
Phagocytosis rates of all of the 73 Klebsiella pneumoniae isolates causing liver abscess from Singapore and Taiwan, classified as four groups: serotype K1 (magA positive and rmpA positive), serotype K2 (magA negative and rmpA positive), rmpA-positive ...

To further verify the result of the phagocytosis assay, a total of 16 isolates were used for mouse inoculation. We randomly chose two of each serotype K1, K2, rmpA-positive non-K1/K2 and rmpA-negative non-K1/K2 strains isolated from Singapore and from Taiwan.

All mice with intraperitoneal injection of serotype K1 or K2 strains died within 2 weeks, while no lethality was observed with rmpA-negative non-K1/K2 strains. Among rmpA-positive non-K1/K2 strains, isolates from Singapore showed no virulence to the mouse model, while those from Taiwan caused the deaths of 10 out of 12 mice within 2 weeks. Except for the rmpA-positive non-K1/K2 group, there was no difference of lethality between isolates from Singapore and Taiwan.

Overall, the K1 or K2 isolates were significantly more virulent in the mouse model than rmpA-positive and rmpA-negative non-K1/K2 isolates (survival rates of 0/48 versus 14/24 [P < 0.0001] and 0/48 versus 24/24, respectively). Among the non-K1/K2 strains, the rmpA-positive group from Taiwan was significantly more virulent in the mouse model than the rmpA-negative group (survival rate of 14/24 versus 24/24) (Fig. (Fig.33).

FIG. 3.
Mouse lethality of 16 Klebsiella pneumoniae isolates causing liver abscess. (A) Eight from Singapore. (B) Eight from Taiwan. Both are comprised of two serotype K1 (magA positive and rmpA positive), two serotype K2 (magA negative and rmpA positive), two ...

DISCUSSION

K. pneumoniae has become the most common pathogen causing pyogenic liver abscesses in Singapore and Taiwan (25). Our present data show that K. pneumoniae isolates from patients with liver abscesses in Singapore and Taiwan have similar characteristics, such as genomic heterogeneity and the prevalence of serotype K1 or K2, magA, and rmpA. However, the virulences of rmpA-positive strains from Taiwan and Singapore were different in the mouse model, indicating that factors other than rmpA contributed to the virulence. This difference mandates further investigation.

Although one group has previously identified a major cluster of K. pneumoniae isolates causing liver abscesses in Taiwan (8), subsequent studies with the methods of ribotyping and PFGE showed that K. pneumoniae-related liver abscesses are not caused by a clonally spread strain in Taiwan (1, 3, 6, 10). In the present study, our PFGE data further confirm that K. pneumoniae isolates causing liver abscesses are not clonal in either Singapore or Taiwan.

magA, serotype K1 or K2, and rmpA have been proposed as good markers for the rapid diagnosis of liver abscess (4, 5). In one study, rmpA and magA were significantly more prevalent in liver abscess isolates than in those from non-liver abscess community-acquired bacteremia (14/16 versus 45/89 [P = 0.006] and 7/16 versus 16/89 [P = 0.02], respectively) (26). Although most K. pneumoniae liver abscess strains had rmpA, 45 of 59 (76%) of rmpA-positive K. pneumoniae isolates causing community-acquired bacteremia were not associated with liver abscess (26). In another study, serotype K1 or K2 showed no significant difference in prevalence between liver abscess and non-liver abscess community-acquired bacteremia (8/22 versus 20/72; P = 0.46) (22). Therefore, none of these three factors appears to be useful for the diagnosis of liver abscess from community-acquired K. pneumoniae bacteremia.

We have previously described magA as unique to serotype K1 isolates among K. pneumoniae strains causing liver abscesses in Taiwan (24). This study shows that this is true for K. pneumoniae in Singapore as well. magA has been confirmed to be located in the cps (capsular polysaccharide synthesis) gene cluster of serotype K1 of K. pneumoniae and is restricted to serotype K1 isolates, regardless of their sources (4, 20, 24). Our present data show that the magA-positive serotype K1 and the magA-negative serotype K2 groups were equally more phagocytosis resistant and virulent than the magA-negative non-K1/K2 group. As magA is restricted to serotype K1 and there were some magA-negative isolates, such as serotype K2, of equal virulence, magA is a good tool for molecular typing rather than a major virulence determinant.

A previous study has documented that rmpA (regulator of mucoid phenotype) was located on a 180-kb virulence plasmid and was responsible for expressing the mucoid phenotype of K. pneumoniae serotype K2 (14). After sequencing of the rmpA-carrying plasmid pLVPK of the serotype K2 CG43 strain, it was found that the plasmid also contained many virulence-associated genes, including rmpA2 (homolog of rmpA), and genes encoding aerobactin for iron acquisition (2). Thus, the presence of rmpA in a K. pneumoniae isolate may suggest that it carries a plasmid containing many other virulence-associated genes. Although previous studies on rmpA were limited to serotype K2 strains, our results showed that rmpA also exists in serotypes other than K2 and all K1/K2 liver abscess isolates carried rmpA. Although we had no rmpA-negative isolates among serotype K1 or K2, this study and a previous report (14) have demonstrated that the rmpA-negative isolates are less phagocytosis resistant and/or less virulent than their rmpA-positive counterparts of the same serotype.

With an almost 90% prevalence rate of rmpA in liver abscess strains, it was not surprising that all of our K1 or K2 isolates and more than half of the non-K1/K2 isolates carried this gene. In our work, the role of rmpA in virulence was confirmed by the higher phagocytosis resistance rate of rmpA-positive non-K1/K2 strains than that of their rmpA-negative counterparts. Although isolates of rmpA-positive non-K1/K2 strains in Taiwan showed high lethality in a mouse model, its importance in virulence was not further confirmed by rmpA-positive non-K1/K2 isolates from Singapore. Besides, among rmpA-positive isolates, the K1 or K2 group has a more significant phagocytosis resistance rate and higher mouse lethality than the non-K1/K2 group. In spite of its highest prevalence in liver abscess and contribution to the phagocytosis resistance of non-K1/K2 strains, rmpA plays a minor role in virulence compared with the presence of serotype K1 or K2 measured by either phagocytosis assay or mouse inoculation.

The importance of K. pneumoniae capsular serotype in virulence and phagocytosis resistance has been reported before (11, 13, 19). We showed that serotype K1 or K2 played a more determinant role in virulence than those of magA and rmpA in liver abscess strains. Although serotype K1 or K2 was not associated with the spontaneous rupture of liver abscess (10), all of the metastatic septic complications were caused by serotype K1 or K2 (6). Serotype K1 or K2 was significantly more prevalent in metastatic strains than in liver abscess strains (18/18 versus 104/134; P < 0.05) (6). It seems that the higher virulence and the higher resistance to phagocytosis render serotype K1 or K2 strains more likely to cause metastatic septic complication.

In conclusion, serotype K1 or K2 is the major virulence determinant for K. pneumoniae liver abscess. There was no regional difference of liver abscess isolates between Singapore and Taiwan. magA correlated to only the K1 capsular serotype. Despite its high prevalence in liver abscess K. pneumoniae isolates, rmpA contributed partially in phagocytosis resistance but was not a major factor for virulence. Serotype K1 or K2, rather than magA and rmpA, correlated best with the virulence of K. pneumoniae isolates causing liver abscess.

Acknowledgments

This work was supported by grants from the National Science Council of Taiwan (NSC-93-2314-B-016-018 and NSC 94-2314-B-016-004).

We would like to thank Ong Lan Huay, Department of Pathology, Singapore General Hospital, for maintaining the isolates during the study period.

Footnotes

[down-pointing small open triangle]Published ahead of print on 6 December 2006.

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