Abstract
Most of the cases of Klebsiella pneumoniae liver abscess reported early on were from Asia, predominantly Taiwan, with a significant number of patients being middle aged diabetic men, and developing metastatic complications, especially endophthalmitis. The entity is now being increasingly recognized in the United States. In this article, the authors review those reported cases, and also the literature regarding the pathophysiology of this intriguing syndrome.
Key Indexing Terms
Introduction
Liver abscess is a relatively common infection caused by a variety of bacterial, fungal and parasitic pathogens. Until recently, Escherichia coli was the most common etiologic agent of pyogenic liver abscesses but starting in the mid 1980s, increasing case reports of Klebsiella pneumoniae liver abscess (KLA) began appearing in the literature. Most of these infections were reported from Taiwan. The patients were middle-aged men with diabetes, with a significant number of them developing bacteremia and metastatic complications, especially endophthalmitis. In the past decade, several cases of KLA have been reported from the United States, with a somewhat similar disease spectrum. We review all the cases that have been reported in the United States so far, and also explore the pathophysiologic mechanisms of this unique disease process.
Methods
We reviewed all the published case reports in the literature of KLA in the United States. This was done by performing a PubMed search, using keywords Klebsiella and liver abscess. Altogether, 34 cases and case series were identified and included in the review. The period of the reviewed articles was from 1949 to date.
Results
Including our case, we found a total of 93 cases of KLA in the United States ( Table). Excluding 1 newborn, all the patients were adults. The age range was from 28-78 years, with a mean age of 53 years. The male-to-female ratio was approximately 3:1. The most common underlying conditions that were reported were diabetes (18 patients), hypertension (14 patients), biliary disease (10 patients) and coronary artery disease (2 patients).
TABLECase reports of liver abscesses due to Klebsiella pneumoniae.
| Case no. | Ref. | Age (years) | Sex/ethnicity | Underlying condition/risk factor | Location of liver abscess | Positive cultures | Serotype | Antibiotic treatment | Procedure | Complications | Outcome |
|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 | 1 | 60 | F/white | Unknown | R lobe, single | Blood, liver, CSF | Unknown | Streptomycin | None | Meningitis | Died |
| 2 | 2 | 51 | F/white | Diabetes | R lobe, single | Blood, CSF | Unknown | Streptomycin/sulfadiazine | None | Meningitis | Died |
| 3 | 3 | Newborn | F/white | Umblical vein catheterization | Unknown | Blood, CSF | Unknown | Unknown | None | Meningitis | Died |
| 4 | 4 | 48 | M/black | Unknown | R lobe, single | Liver | Unknown | Unknown | Open drainage | Tibial osteomyelitis | Survived |
| 5 | 5 | 70 | F/white | Pancreatic cancer s/p Whipple procedure | Diffuse hepatitis | Blood, liver | Unknown | Penicillin/gentamicin | Surgical exploration with liver biopsies | None | Survived |
| 6 | 6 | 68 | F/hispanic | Diabetes, HTN, CHF | L lobe, multiple | Liver | Unknown | Ampicillin/gentamicin | Open drainage | None | Survived |
| 7 | 7 | 33 | M/white | Unknown | R lobe, single | Liver | Unknown | Unknown | Percutaneous drainage | None | Survived |
| 8 | 8 | 37 | M/white | Hemorroidectomy | L lobe, single | Blood, liver | Unknown | Penicillin/gentamicin/metronidazole | Percutaneous drainage | None | Survived |
| 9 | 9 | 50 | M/white | Choledocholithiasis | Both lobes, multiple | Blood | Unknown | Cefazolin | Common bile duct stent | None | Survived |
| 10–14 | 10 | Unknown | Unknown | “Benign biliary disease” (1) | Unknown | Not specified | Unknown | Not specified | Not specified | Not specified | Not specified |
| “Malignant biliary disease” (2) | |||||||||||
| Pancreatitis (1) | |||||||||||
| Unknown (1) | |||||||||||
| 15 | 11 | 61 | M/not specified | None | R lobe, single | Blood, liver | Unknown | Ceftizoxime/ | Percutaneous drainage | Pneumonia | Survived |
| Metronidazole | Endophtalmitis | (Needed eye prosthesis) | |||||||||
| 16 | 12 | 38 | M/black | Diabetes | R lobe, single | Liver, CSF | Unknown | Ceftriaxone/ | Percutaneous drainage | Meningits | Survived |
| Metronidazole, then | Endophthalmitis | ||||||||||
| Levofloxacin/Metronidazole | |||||||||||
| 17 | 13 | 32 | M/not specified | Beta-thalassemia major | R lobe, multiple | Liver, vitreous | Unknown | Ceftriaxone/ | Percutaneous drainage | Subretinal abscess | Survived |
| Splenomegaly | Gentamicin/ | Vitrectomy, retinectomy | Renal abscess | (Vision 20/30) | |||||||
| Metronidazole, then Ciprofloxacin | |||||||||||
| 18 | 14 | 57 | M/black | Diabetes, cystic duct obstruction | Both lobes, multiple | Blood, liver | Unknown | Ciprofloxacin/ | Open drainage | None | Survived |
| Clindamycin | Cholecystectomy | ||||||||||
| 19 | 15 | 29 | M/not specified | None | R lobe, single | Blood, liver | Unknown | Piperacilin/tazobactam | Percutaneous drainage | None | Survived |
| 20 | 62 | M/white | Diabetes | R lobe, single | Blood, liver | Unknown | Ciprofloxacin/imipenem | Percutaneous drainage | None | Survived | |
| 21–43 | 17 | Not specified | Asian/hispanic | Not specified | Not specified | Liver | Unknown | Varied | Not specified | None | Overall 2.5% mortality |
| 44 | 18 | 62 | M/white | Diabetes | R lobe, single | Blood, liver | K-1 | Quinolone | Percutaneous drainage | None | Survived |
| 45–50 | 19 | 50–71 | 4 Men/2 women | ||||||||
| 2 White | Coronary artery disease | L lobe, single (2) | Blood, liver (2) | Unknown | Cephalosporin/ | Percutaneous drainage | None | Survived | |||
| 4 Filipino | Diabetes, CAD, HTN | Both lobes, multiple (1) | Blood, liver (3) | metronidazole | in all 6 patients | ||||||
| L lobe, multiple (1) | Liver (1) | ||||||||||
| L lobe, single (1) | Quinolone/ | ||||||||||
| R lobe, single (1) | metronidazole | ||||||||||
| 51–52 | 20 | 49 | M/Hawaiian | Diabetes | R lobe, single | Liver | Unknown | Ciprofloxacin/metronidazole | Percutaneous drainage | Septic shock | Survived |
| 56 | M/Hawaiian | Diabetes | Both lobes | Liver | Unknown | Ceftriaxone/metronidazole, then Amoxicillin-clavulanate | Percutaneous drainage | None | Survived | ||
| 53 | 21 | 65 | M/not specified | Acute lymphocytic leukemia | Both lobes, multiple | Liver | Unknown | Cefepime | Percutaneous drainage | None | Survived |
| 54 | 22 | 49 | M/not specified | Not specified | R lobe, single | Liver | Unknown | Ceftriaxone/ciprofloxacin/metronidazole | Percutaneous drainage | Hepatobronchial fistula | Survived |
| 55 | 23 | 42 | M/Filipino | None | R lobe, single | Liver, CSF | Unknown | Ceftriaxone/metronidazole | Percutaneous drainage | Meningitis | Survived |
| Septic emboli to brain and lung | |||||||||||
| 56 | 24 | 42 | M/Vietnamese | Diabetes | R lobe, multiple | Liver, blood, sputum, urine, neck abscess | K-1 | Imipenem/levofloxacin | Percutaneous drainage | Neck abscess | Survived |
| Lung abscess | |||||||||||
| 57 | 25 | 43 | M/Haitian | None | R lobe, single | Liver, vitreous | Unknown | Gatifloxacin | Percutaneous drainage | Endopthalmitis | Survived |
| Preseptal abscess | (Required enucleation) | ||||||||||
| 58–77 | 26 | Median 56.5 | 14 Men, 6 Women | Hypertension (9) | R lobe, single (15) | Blood (13) | Unknown | Ceftriaxone | Percutaneous drainage | Emboli to lungs (4) | Survived (18) |
| 12 Asian descent | Diabetes (5) | L lobe, single (1) | Liver (14) | Ciprofloxacin | (16 Patients) | Meningitis (1) | Died (2) | ||||
| 8 Hispanic descent | Biliary disease (5) | R lobe, multiple (2) | Blood and liver (8) | Open drainage | Endophthalmitis (1) | ||||||
| None (4) | L lobe, multiple (2) | (2 Patients) | Pneumonia (1) | ||||||||
| 78 | 27 | 28 | M/not specified | None | R lobe, multiple | Blood, liver | Unknown | Ceftriaxone | None | Septic emboli to lungs | Survived |
| 79 | 28 | 51 | M/not specified | None | Not specified | Blood, liver, vitreous, urine | Unknown | Not specified | Percutaneous drainage | Endophthalmitis | Survived |
| (Required enucleation) | |||||||||||
| 80 | 29 | 49 | M/Afro-Caribbean | None | R lobe, multiple | Liver, blood | K-2 | Ceftriaxone | Percutaneous drainage | Brain abscesses | |
| 81–87 | 30 | Not specified | Not specified | Not specified | Not specified | Liver | Rmp+ | Not specified | Not specified | Not specified | Not specified |
| 88 | 31 | 39 | M/Filipino | None | R lobe, single | Liver, mitral valve | K-2 | Ceftriaxone | Mitral valve replacement | Endophthalmitis | Survived |
| Endocarditis | |||||||||||
| Septic emboli to lungs | |||||||||||
| 89 | 32 | 58 | F/not specified | None | R lobe, single | Liver | Unknown | Piperacillin-tazobactam, then ciprofloxacin | Percutaneous drainage | None | Survived |
| 90 | 33 | 78 | M/not specified | DM, HTN, PAD, A Fib, | R lobe, single | Liver | K-1 | Ceftriaxone | Percutaneous drainage | None | Survived |
| 91–92 | 34 | 53 | F/African-American | Not specified | Not specified | Liver | K-29 | Not specified | Not specified | None | Survived |
| 52 | M/Chinese | Diabetes, HTN | R lobe, single | Liver, blood | K-1 | Not specified | Not specified | None | Survived | ||
| 93 | Our case | 68 | M/Bangladeshi | Diabetes, HTN, prostate cancer | R lobe, multiple | Liver, blood | Unknown | Ceftriaxone/metronidazole | Percutaneous drainage followed by R lobe lobectomy | Multiorgan failure | Died |
A Fib, atrial fibrillation; CAD, coronary artery disease; CHF, congestive heart failure; CSF, cerebrospinal fluid; DM, diabetes mellitus; HTN, hypertension; PAD, peripheral artery disease.
Among the patients with ethnicity reported, the distribution was as follows: Asian (39 patients), Hispanic (16 patients), White (12 patients), African-American (4 patients) and Hawaiian (2 patients).
In patients who had the location of the abscess reported, the right lobe of the liver was more commonly affected (34 patients with single lesion and 7 patients with multiple lesions). The left lobe was less frequently involved (5 patients with single lesion and 4 patients with multiple lesions), whereas multiple lesions in both the lobes were reported only in 4 patients.
Cultures were positive from the liver abscess in 73 (78%) patients, blood in 43 (46%) patients and both blood and liver abscess in 27 (29%) patients. Other less frequently involved sites with positive cultures were the cerebrospinal fluid (4 patients), vitreous (3 patients), urine (2 patients) and sputum, soft tissue abscess of the neck and mitral valve (1 patient each). Only 7 patients had a polymicrobial infection, and the other bacteria involved were Enterococcus fecalis and Clostridium perfringens. The serotypes of the isolates were unknown for most patients (85 patients). Among the 8 patients in whom serotyping was done, 4 patients were reported as K-1 positive, 2 patients as K-2 positive and 1 each patient as K-29 and Rmp A positive.
In the pre-1970 era, the antibiotics used were streptomycin, and penicillin or ampicillin with gentamicin. In the post-1970 era, the most frequently used combination was ceftriaxone and metronidazole. From the 1990s onwards, a quinolone with metronidazole was the next most common combination used.
Complications were not infrequently encountered in the patients in our review. The reported complications were endophthalmitis (7 patients), meningitis (6 patients), septic emboli to the lungs (4 patients) and pneumonia (2 patients). Less frequently encountered complications were renal abscess, lung abscess, septic emboli to brain, brain abscess, endocarditis, hepatobronchial fistula and tibial osteomyelitis (1 patient each). Of the 7 patients who had endophthalmitis, 3 patients required surgical intervention (enucleation/eye prosthesis). The overall mortality was 7%. However, 2 of the patients who died were from early case reports (late 40s-early 50s).
Discussion
Pyogenic liver abscess can be either bacterial or fungal in etiology. In the developed world, pyogenic liver abscess constitutes three-fourths of all liver abscesses, with an incidence of 1 in every 4,500–7,000 hospital admissions.
19
There are several routes via which infection can reach the liver, leading to the development of an abscess. These include the portal vein, biliary tree, hepatic artery, direct extension of infection and penetrating trauma. In the pre- and early antibiotic era, pylephlebitis due to abdominal visceral infection, especially appendicitis, was the most common cause of liver abscess formation. Appendicitis rarely causes liver abscess now because of the use of early, broad-spectrum antibiotics. Biliary tract infection is now the leading cause of secondary bacterial liver abscess. Infections like diverticulitis, colitis and pancreatitis continue to remain important causes, although the incidence of liver abscesses due to these appears to be decreasing. In a significant number of patients, no cause is apparent. These primary cryptogenic abscesses have been reported as the predominant category in several case series.Up to the 1980s, E. coli was the most common etiologic agent, usually found in the setting of a polymicrobial infection with a bowel or biliary source. Beginning in the mid 1980s, primary liver abscesses without intra-abdominal or biliary tract infection began to be reported in the literature.
35
The patients were mostly middle-aged Southeast-Asian men, with a significant number having underlying diabetes or impaired glucose tolerance. Bacteremia and metastatic complications were frequent, especially endophthalmitis and meningitis.36
KLA has since been reported from several other countries including Korea, Singapore, Thailand, Japan, Spain, England and Australia. Cases have been reported from the United States sporadically but the frequency seems to have increased over the past 2 decades.We reviewed all cases of KLA reported in the United States so far and found a total of 93 patients. Almost half of the patients were of Asian descent and only a small fraction of patients were White. A smaller percentage of patients in our review had diabetes compared to the studies from Vietnam. The mean age, male-to-female ratio, predominance of the right lobe of the liver, bacteremia, metastatic complications (especially meningitis and endophthalmitis) and mortality were similar to those reported in the Vietnamese studies.
35
, 36
Serotyping data were available only in a small number of patients; most of them had the K1/K2 serotype. The treatment modality used uniformly was percutaneous drainage accompanied by antibiotics. A third generation cephalosporin and metronidazole was the preferred regimen both in the United States and Vietnam, whereas several patients in the United States (in the last 2 decades) were treated with a fluoroquinolone and metronidazole. Our patient was male, diabetic and of Asian descent. His liver abscess seems to have been the primary source of infection without any other obvious foci or metastatic complications like meningitis and endophthalmitis. Unfortunately, serotyping could not be performed. As our review included cases over a long period of time, it is possible that there could have been bias in certain characteristics, like the incidence of underlying diabetes and other chronic medical comorbidities, as well as the ethnicity of the patients.
KLA seems to be a unique syndrome that is being increasingly recognized worldwide. It is frequently complicated by bacteremia, sepsis and metastatic spread of infection. As mentioned earlier, most of the early cases were reported from Taiwan. In a large series, Wang et al
37
retrospectively reviewed a total of 182 cases of pyogenic liver abscess in Taiwan from 1990–1996. Of these, 160 cases were due to K. pneumoniae alone and 22 cases were polymicrobial. As compared to patients with polymicrobial infection, the authors found patients with KLA to have increased incidence of diabetes or glucose intolerance (75% versus 4.5%) and metastatic infection (11.9% versus 0%), and lower rate of intra-abdominal abnormality (0.6% versus 95.5%), relapse (4.4% versus 41%) and mortality (11.3% versus 41%). A subsequent study, also from Taiwan, showed similar results.38
Out of a total of 248 cases of pyogenic liver abscesses, K. pneumoniae was the causative agent in 171 (69%) cases. Abscesses caused by K. pneumoniae were found to have a stronger association with diabetes or impaired fasting glucose (70% versus 32%), metastatic infection (14% versus 4%) and lower mortality (4% versus 21%).The pathogenesis of the KLA syndrome is still not completely understood. One of the leading host factors that has been implicated is diabetes or impaired glucose tolerance. Most studies have reported a high prevalence of diabetes or impaired glucose tolerance, some of them of more than 70%, although this is not universal. Impaired glycemic control is believed to result in decreased neutrophil phagocytosis, especially of K1 and K2 capsular serotypes.
Fatty liver has also been reported more frequently with KLA than with liver abscesses due to other bacteria, although this association is not as strong as diabetes or impaired glucose tolerance.
39
Given the high prevalence of KLA in Asians and patients living in other countries of Asian descent, a genetic predisposition to KLA is suspected, although not proven. Chinese ethnicity might be associated with a higher likelihood of intestinal colonization with K. pneumoniae isolates of the K1 and K2 serotypes. In a study examining K. pneumoniae from the stool of healthy Chinese adults living in 8 different Asian countries, K1 and K2 serotypes accounted for 10% of the isolates.
40
Obviously, more research is needed to derive conclusive inferences in this regard.There are 77 capsular polysaccharide (CPS) antigens of K. pneumoniae. The K1 and to a lesser degree, K2 strains are thought to be the most virulent, and have been the most frequently reported in KLA. The following virulence factors have been implicated: (1) thick encapsulation of K1 and K2 strains, (2) resistance to phagocytosis, (3) magA (mucoviscosity associated gene A) and (4) rmpA (regulator of mucoid phenotype A gene).
Animal studies carried out approximately 20 years ago revealed that CPS (K antigen) is the main virulence factor for K. pneumoniae.
41
, 42
Serotypes K1 and K2 were found to be the most virulent in these animal models. Fung et al43
were the first to demonstrate similar findings in humans. They reviewed 134 cases of KLA in Northern Taiwan from 1991–1998. Serotyping of the isolates revealed that K1 (85/134; 63%) and K2 (19/134; 14%) were the most common. Septic endophthalmitis was reported in 14 (10%) of the 134 patients. K1 serotype was found in 85% of these patients (12/14) and K2 in 14% (2/14). Liver, blood and vitreous cultures revealed the same serotype in all 14 cases.Fang et al
44
reported a study of 177 patients with KLA at a tertiary university hospital in Taiwan from 1997–2005. Septic ocular or central nervous system complications were found in 23 (13%) patients. Presence of serotype K1 was the only significant risk factor for the development of these complications. K1 isolates were found to be significantly more virulent than non-K1 isolates based on serum resistance assays. Other than the serotype-specific CPS synthesis (cps) region, the genomic background of the K1 strains also differed compared to non-K1 strains (presence of 20-kb kfu/PTS region in the K1 strains). In the 19 cases in which K1 strains caused complications, 8 (42%) patients had no underlying medical disease, suggesting that this serotype can cause metastatic complications even in otherwise healthy individuals.To elucidate the role of CPS in KLA and the development of metastatic endophthalmitis, Lin et al
45
studied neutrophil phagocytosis of 70 CPS isolates (K1 [n = 23], K2 [n = 10] and non-K1/K2 [n = 37]), using flow cytometry, fluorescence imaging and electron microscopy. These isolates had been previously obtained from patients with systemic infections, including liver abscess. The authors found that the K1/K2 isolates were more resistant to phagocytosis and showed increased resistance to intracellular killing, which likely leads to their increased propensity for liver abscess and endophthalmitis.K. pneumoniae isolates causing the KLA syndrome exhibit a hypermucoviscosity phenotype. This is evident in the microbiology laboratory by the presence of mucoid colonies and the “string sign” on culture plates. The chromosomal magA gene and the plasmid-mediated rmpA gene are believed to be responsible for this phenotype.
Chuang et al
46
tried to ascertain the genetic determinants of K1 serotype causing KLA. A total of 35 of 42 isolates from patients with KLA were magA positive, whereas only 1 of 32 non-KLA isolates was magA positive. All the 36 magA-positive strains were serotype K1, whereas none of the magA-negative strains were of the K1 serotype. Sequencing of the magA flanking region revealed a cps region containing 20 open-reading frames; of these, 9 isolates were cotranscribed as part of an operon. The authors hypothesized that an operon containing magA is responsible for capsular serotype K1 and that several loci in the operon are determinants of this particular serotype.In addition to magA, there is evidence that rmpA also contributes to the hyperviscous phenotype and virulence of K1 serotypes. In the earlier mentioned study by Fang et al,
44
K1 strains had a higher mean number of rmpA copies per strain than non-K1 isolates. Yu et al47
looked at 151 K. pneumoniae blood stream isolates, and found the prevalence of hypermucoviscosity, rmpA and magA to be 38% (58 of 151 isolates), 48% (72 of 151 isolates) and 17% (26 of 151 isolates), respectively. Of the 58 hypermucoviscosity-positive isolates, 52 (90%) isolates were rmpA positive and 17 (29%) isolates were magA positive.Hyperviscosity was predicted by 52 (72%) of 72 of the rmpA-positive strains and 17 (65%) of 26 of the magA-positive strains. Presence of rmpA and magA in the same isolate increased the expression of the hypermucoviscous phenotype. This study suggests that rmpA could be responsible for the hypermucoviscosity phenotype in magA-negative isolates like K2 and other non-K1 strains.
To explore the correlation of capsular serotype, magA and rmpA with virulence, Yeh et al
48
reviewed 73 KLA isolates from Singapore and Taiwan. The most common serotypes were K1 (34/73; 47%) and K2 (15/73; 20%). As expected, magA was present only in the K1 isolates. All K1 and K2 isolates, and two-thirds of the non-K1/K2 isolates carried rmpA. K1 and K2 isolates showed more virulence and phagocytic resistance than rmpA-positive and rmpA-negative non-K1/K2 isolates. These findings suggest that capsular serotype K1 or K2, rather than magA and rmpA, plays a more important role in virulence of K. pneumoniae causing liver abscess.A more recent study tried to elucidate predictors of septic metastatic infection and mortality in patients with KLA.
49
The presence of rmpA, Acute Physiologic and Chronic Health Evaluation II score ≥20, and septic shock were significant risk factors for metastatic infection. In addition, the authors found the following to be predictors of mortality: metastatic infection, Acute Physiologic and Chronic Health Evaluation II score ≥16, septic shock, acute respiratory failure and presence of gas on abdominal imaging.KLA with metastatic infection is a unique syndrome initially described in Southeast Asia, with increasing number of cases now being reported in the United States. Diabetes seems to be a less prominent risk factor in the United States. Hypermucoviscosity and serotypes K1/K2 with presence of rmpA and magA genes appear to be most commonly associated with this syndrome. Septic ocular and central nervous system complications are frequently encountered, which can lead to significant morbidity. The disease pattern appears to be similar to that reported in Southeast Asia. It is still somewhat unclear whether there is a genetic predisposition in patients of Asian ancestry to the KLA syndrome, even if they have lived in the United States. Nonetheless, physicians in the United States need to be aware of this syndrome to optimize management.
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Article info
Publication history
Accepted:
October 8,
2015
Received:
June 18,
2015
Footnotes
☆The authors have no conflicts of interest to disclose.
Identification
Copyright
Published by Elsevier Inc.
