Published online Apr 27, 2024. doi: 10.4254/wjh.v16.i4.612
Peer-review started: December 29, 2023
First decision: January 23, 2024
Revised: February 1, 2024
Accepted: March 8, 2024
Article in press: March 8, 2024
Published online: April 27, 2024
Processing time: 116 Days and 18.1 Hours
Liver transplantation (LT) is the only curative treatment for end-stage liver disea
To assess KPI incidence, timing, distribution, drug resistance, and risk factors following LT and its association with outcomes.
This retrospective study included 406 patients undergoing LT at The Third Xiangya Hospital of Central South University, a tertiary hospital, from January 2015 to January 2023. We investigated the risk factors for KPIs and assessed the impact of KPIs and CRKP infections on the prognosis of LT recipients using logistic regression analysis.
KPI incidence was 7.9% (n = 32), with lung/thoracic cavity the most frequent site of infection; the median time from LT to KPI onset was 7.5 d. Of 44 Klebsiella pneumoniae isolates, 43 (97.7%) and 34 (77.3%) were susceptible to polymyxin B or ceftazidime/avibactam and tigecycline, respectively; > 70% were resistant to piperacillin/ tazobactam, ceftazidime, cefepime, aztreonam, meropenem, and levofloxacin. Female sex [odds ratio (OR) = 2.827, 95% confidence interval (CI): 1.256-6.364; P = 0.012], pre-LT diabetes (OR = 2.794, 95%CI: 1.070-7.294; P = 0.036), day 1 post-LT alanine aminotransferase (ALT) levels ≥ 1500 U/L (OR = 3.645, 95%CI: 1.671-7.950; P = 0.001), and post-LT urethral catheter duration over 4 d (OR = 2.266, 95%CI: 1.016-5.054; P = 0.046) were risk factors for KPI. CRKP infections, but not KPIs, were risk factors for 6-month all-cause mortality post-LT.
KPIs occur frequently and rapidly after LT. Risk factors include female sex, pre-LT diabetes, increased post-LT ALT levels, and urethral catheter duration. CRKP infections, and not KPIs, affect mortality.
Core Tip: Despite advances in liver transplantation (LT) technology, Klebsiella pneumoniae infections (KPIs) remain challenging to treat. Timely prevention of KPIs is therefore critical. Many risk factors play crucial roles in the occurrence of KPIs after LT and in determining recipient prognosis. We examined the role of KPIs in the prognosis of LT recipients and the risk factors for KPIs after LT. By analyzing the distribution of KPIs and drug resistance, we demonstrated that risk factors are associated with surgical operative variables. Identifying these risk factors provides a basis for preventing KPIs, which, in turn, may improve the prognosis of LT recipients.
- Citation: Guo L, Peng P, Peng WT, Zhao J, Wan QQ. Klebsiella pneumoniae infections after liver transplantation: Drug resistance and distribution of pathogens, risk factors, and influence on outcomes. World J Hepatol 2024; 16(4): 612-624
- URL: https://www.wjgnet.com/1948-5182/full/v16/i4/612.htm
- DOI: https://dx.doi.org/10.4254/wjh.v16.i4.612
Liver transplantation (LT) is the only curative treatment for end-stage liver disease[1]. However, the lifelong use of immunosuppressant drugs makes LT recipients susceptible to infection, which is the most common cause of early mortality after LT[2]. In recent years, studies have demonstrated that infections in LT recipients are more likely to be caused by gram-negative than gram-positive pathogens[3]. The gram-negative bacterium Klebsiella pneumoniae (K. pneumoniae) is a common cause of infection, with reports indicating that 6.9%-14.2% of LT recipients experienced bloodstream infections caused by this pathogen[4,5].
The major concern regarding K. pneumoniae infections (KPIs) is the incidence of carbapenem-resistant K. pneumoniae (CRKP), which ranges from 2.5% to 35%; CRKP-associated mortality is as high as 35%-83% among LT recipients[5-12]. Therapeutic options for these infections are limited.
Although some studies have demonstrated the effects of CRKP infection on the prognosis of solid organ transplant (SOT) recipients, the impact of KPIs or CRKP infections in LT recipients remains unclear[5,13,14]. The present study examined the drug resistance and distribution of K. pneumoniae isolates and the effect of KPIs, particularly CRKP infections, on outcomes after LT. The findings of this study should provide clues for preventing KPIs and improving the outcomes of LT recipients with KPIs.
We conducted a single-center retrospective study including all adult patients who underwent LT at The Third Xiangya Hospital of Central South University from January 1, 2015, to January 31, 2023. Four patients with donor-derived KPIs and two patients aged under 18 years were excluded from the analysis, along with two patients who died within 48 h of transplantation due to massive intraoperative blood loss or primary graft nonfunction. Finally, 405 patients who received donations after brain death and 1 patient who received a donation after circulatory death were included in the analysis. All LT recipients underwent modified piggyback LT. Induction immunosuppression consisted of corticosteroids with or without basiliximab, and maintenance immunosuppression involved a corticosteroid taper and tacrolimus/cyclosporin A with or without mycophenolate mofetil or enteric-coated mycophenolate sodium. Standard perioperative antibacterial prophylaxis consisted of third-generation cephalosporins or carbapenems administered for 3-5 d. Teicoplanin, caspofungin, and other antibiotics were prescribed according to the infection status and identified pathogens. Antithymocyte globulin was prescribed when acute rejection episodes were not resolved by glucocorticoid therapy or when glucocorticoids were unsuitable for preventing acute rejection. This study was approved by the Ethics Committee of The Third Xiangya Hospital (approval number: 24029) and conducted in accordance with the principles outlined in the Declaration of Helsinki.
All patients were routinely followed-up in the outpatient department post-LT. The clinical data of LT recipients aged ≥ 18 years were extracted from inpatient and outpatient electronic medical records, including demographic information and infection characteristics. The follow-up periods were 3 months for microbiological data and 6 months for mortality. We also analyzed the prevalence of KPIs and CRKP infections and lengths of intensive care unit (ICU) and hospital stays after LT. Analysis was performed to identify risk factors for KPIs, 6-month all-cause mortality, and ICU stays of at least 7 d after LT.
Infections were defined using the standards of the Centers for Disease Control and Prevention/National Healthcare Safety Network[13]. Infection was confirmed based on a positive culture together with clinical signs of an active infection, including chills, fever, hypotension, or imaging findings from computed tomography or chest radiography. The source of infection was confirmed by a positive culture accompanied by clinical manifestations[13]. CRKP was defined as an insusceptibility to at least one carbapenem, with a minimum inhibitory concentration of ≥ 4 µg/mL for imipenem or meropenem (Clinical and Laboratory Standards Institute, 2017). Reoperations included both retransplantation and post-LT laparotomy. Acute rejection was determined by biopsy.
Patient samples, including blood, sputum, bronchoalveolar lavage fluid, urine, ascites, bile, organ preservation solution, and catheter drainage fluid, were collected for clinical bacterial culture. Sputum samples were obtained from the trachea or were induced. Blood, urine, sputum, and abdominal drainage fluid were subject to routine bacterial culture once a day for 5-7 d after LT. Samples were collected for culture when an infection was suspected within the 3 months following LT. Blood samples were cultured and analyzed using a BD9240 automatic blood culture instrument (BD, Franklin Lakes, NJ, United States).The identification and susceptibility tests for culture-positive cases were conducted according to standard bacteriological procedures using a Bruker mass spectrometer and VITEK® 2 system (bioMérieux, Marcyl’Étoile, France). The minimum inhibitory concentration as measured by agar dilution was used to assess the antimicrobial susceptibility of the bacteria. When analyzing drug resistance, all intermediates were classified as resistant.
Statistical analysis was performed using SPSS software version 26.0 (IBM Corporation, Armonk, NY, United States). Categorical variables are expressed as frequencies and percentages. Continuous variables with and without normal distributions are expressed as means ± SD and medians and interquartile ranges, respectively. Chi-squared tests or Fisher’s exact tests were used to compare categorical variables. Binary logistic regression based on forward stepwise regression was used to identify risk factors using odds ratios (OR) and 95% confidence intervals (CI). Risk factors with P-values < 0.01 after univariate analysis were included in the multivariate analysis. Two-tailed P-values < 0.05 were considered statistically significant.
The 406 LT recipients included in the analysis had a mean age of 47.3 ± 10.6 years with a median Model for End-Stage Liver Disease (MELD) score of 23.0; 17.7% of patients were female. Liver failure occurred as a result of hepatitis virus-related cirrhosis/necrosis/tumor (n = 304), alcoholic liver disease (n = 31), mixed cirrhosis (n = 19), autoimmune hepatitis (n = 15), primary biliary cirrhosis (n = 11), cryptogenic cirrhosis (n = 9), Budd-Chiari syndrome (n = 5), hepatolenticular degeneration (n = 3), failure of previous LT (n = 3), drug-induced liver injury (n = 2), polycystic liver (n = 2), and familial hereditary amyloidosis (n = 2). Prior to LT, patients had a median creatinine level of 0.8 mg/dL, albumin level of 34.5 g/L, white blood cell count of 5.2 × 109/L, lymphocyte count of 0.8 × 109/L, and platelet count of 72.0 × 109/L. Two months before LT, 160 (39.4%) patients experienced infections, with 140 (34.5%) experiencing pulmonary infections and 13 (3.2%) experiencing multiple-site infections, all of which involved the lungs. The median surgical time, blood loss, and number of red blood cell (RBC) transfusions were 378.5 min, 3000.0 mL, and 12.0 units, respectively. In the 3 months following LT, 32 (7.9%) patients were infected with 44 strains of K. pneumoniae; 21 (65.6%) patients were infected with CRKP. The median time from transplantation to KPI onset was 7.5 d. After LT, 18 (4.4%) and 395 (97.3%) patients were treated with anti-thymocyte immunoglobulin and tacrolimus, respectively. The median alanine aminotransferase (ALT) and albumin levels on day 1 and the median creatinine level on day 3 after LT were 694.5 U/L, 37.2 g/L, and 0.9 mg/dL, respectively. Overall, 94 patients required mechanical ventilation, 19 required renal replacement therapy, and 67 experienced acute rejection after LT. Moreover, 17 (4.2%) patients underwent reoperation. The median postoperative ICU and hospital stays were 6.0 and 26.0 d, respectively. The 6-month mortality rate was 7.9% (n = 32). Rates of KPI and CRKP infection were significantly higher in patients who died (both 18.8%; n = 6/32) than in those who survived (7.0%; n = 26/374 and 4.0%; n = 15/374, respectively). The baseline demographic, clinical, and laboratory characteristics are summarized in Table 1.
Characteristics | Value |
Recipient age (yr), mean ± SD | 47.3 ± 10.6 |
Recipient gender, no. of female (%) | 72 (17.7) |
Recipient BMI, median (IQR), kg/m2 | 22.8 (20.8-25.1) |
Hospital stay prior to LT, median (IQR), days | 10.0 (1.0-22.3) |
MELD score at LT, median (IQR) | 23.0 (15.0-30.0) |
Infection within 2 months prior to LT, n (%) | 160 (39.4) |
Pulmonary infection | 140 (34.5) |
Abdominal/biliary infection | 6 (1.5) |
Urinary tract infection | 1 (0.2) |
Multiple site infection1 | 13 (3.2) |
Pre-LT use of broad-spectrum antibiotics | 166 (40.9) |
Underlying liver diseases, n (%) | 406 (100) |
Viral cirrhosis/necrosis/tumor | 304 (74.9) |
Alcoholic cirrhosis | 31 (7.6) |
Autoimmune hepatitis | 15 (3.7) |
Primary biliary cirrhosis | 11 (2.7) |
Mixed cirrhosis | 19 (4.7) |
Others2 | 26 (6.4) |
Pre-LT type 2 diabetes, n (%) | 48 (11.8) |
Pre-LT creatinine, median (IQR), mg/dL | 0.8 (0.7-1.0) |
Pre-LT WBC count, median (IQR), × 109/L | 5.2 (3.4-8.1) |
Pre-LT lymphocyte count, median (IQR), × 109/L | 0.8 (0.5-1.2) |
Pre-LT platelet count, median (IQR), × 109/L | 72 (43.8-106.5) |
Pre-LT albumin level, median (IQR), g/L | 34.5 (30.9-38.1) |
Donor age (yr), mean ± SD | 42.1 ± 13.0 |
Steatosis ≥ 30%, n (%) | 42 (10.3) |
Cold ischemia time, mean ± SD | 6.2 ± 1.5 |
Duration of surgery, median (IQR), min | 378.5 (333.0-425.0) |
Intraoperative bleeding, median (IQR), mL | 3000.0 (2000.0-5000.0) |
Intraoperative RBC transfusion, median (IQR), units | 12.0 (8.0-18.0) |
Post-LT infections due to Klebsiella pneumoniae, n (%) | 32 (7.9) |
Post-LT infections due to CRKP, n (%) | 21 (5.2) |
Median interval between the onset of infections due to Klebsiella pneumoniae and LT, median (IQR), days | 7.5 (2.0-17.8) |
Post-LT immunosuppressant treatment, n (%) | 406 (100) |
Tacrolimus | 395 (97.3) |
Ciclosporin A | 5 (1.2) |
Mycophenolate mofetil/enteric-coated mycophenolate sodium | 277 (68.2) |
Sirolimus | 5 (1.2) |
Glucocorticoid | 406 (100) |
Basiliximab | 214 (52.7) |
Anti-thymocyte globulin | 18 (4.4) |
ALT on day 1 after LT, median (IQR), U/L | 694.5 (383.0-1242.0) |
Creatinine on day 3 after LT, median (IQR), mg/dL | 0.9 (0.7-1.4) |
Albumin level on day 1 after LT, median (IQR), g/L | 37.2 (33.9-40.7) |
Post-LT duration of urethral catheter, median (IQR), days | 3.0 (2.0-5.0) |
Post-LT mechanical ventilation, n (%) | 94 (23.2) |
Reoperation, n (%) | 17 (4.2) |
Acute rejection, n (%) | 67 (16.5) |
Post-LT renal replacement therapy, n (%) | 19 (4.7) |
ICU stay after LT, median (IQR), days | 6.0 (5.0-7.0) |
Hospitalization stay after LT, median (IQR), days | 26.0 (21.0-30.0) |
All-cause mortality within 6 months after LT, n (%) | 32 (7.9) |
The most common site of KPI was the lung/thoracic cavity (n = 15), followed by the bloodstream (n = 12) and abdominal/ biliary tract (n = 12) (Table 2).
Infection sites | Lung/thoracic cavity | Blood stream | Abdominal/biliary tract | Urinary tract | Perianal abscess | Liver abscess |
Klebsiella pneumoniae (44) | 15 | 12 | 12 | 3 | 1 | 1 |
The KPIs were resistant to the following antibiotics, from the highest to lowest rate: Piperacillin/tazobactam, levofloxacin, aztreonam, meropenem, cefepime, ceftazidime, cefoperazone/sulbactam, amikacin, trimethoprim/sulfame
Antimicrobial | n | Percentage |
TZP | 34 | 77.3 |
CAZ | 31 | 70.5 |
CFS | 30 | 68.2 |
FEP | 31 | 70.5 |
ATM | 31 | 70.5 |
MEM | 31 | 70.5 |
AN | 21 | 47.7 |
LVF | 33 | 75.0 |
SXT | 20 | 45.5 |
TIC | 10 | 22.7 |
POL | 1 | 2.3 |
CAZ/AVI | 1 | 2.3 |
Univariate logistic regression analysis of patients with and without KPIs identified female sex (P = 0.002), duration of surgery ≥ 450 min (P = 0.033), ALT level ≥ 1500 U/L 1 d after LT (P < 0.001), duration of post-LT urethral catheterization over 4 d (P = 0.009), and post-LT mechanical ventilation (P = 0.015) as risk factors for post-LT KPIs. A MELD score ≥ 22 at LT (P = 0.066), pre-LT diabetes (P = 0.067), infection in the 2 months prior to LT (P = 0.098), and anti-thymocyte globulin use (P = 0.063) showed a trend toward a higher incidence of KPIs but did not reach significance.
Multivariate analysis identified female sex (OR = 2.827, 95%CI: 1.256-6.364; P = 0.012), pre-LT diabetes (OR = 2.794, 95%CI: 1.070-7.294; P = 0.036), ALT level ≥ 1500 U/L 1 d after LT (OR = 3.645, 95%CI: 1.671-7.950; P = 0.001), and post-LT urethral catheter duration over 4 d (OR = 2.266, 95%CI: 1.016-5.054; P = 0.046) as independent risk factors for the development of post-LT KPIs. All data from the univariate and multivariate analyses are presented in Table 4.
Variables | With K. pneumoniae infections(32) | Without K. pneumoniae infections(374) | P value | OR (95%CI) |
Total | ||||
Univariate analysis | ||||
Female sex | 12 (37.5) | 60 (16.0) | 0.002 | |
Recipient age ≥ 55 yr | 10 (31.3) | 91 (24.3) | 0.385 | |
Recipient BMI ≥ 25 | 9 (28.1) | 97 (25.9) | 0.787 | |
MELD score at LT ≥ 22 | 23 (71.9) | 206 (55.1) | 0.066 | |
Hospital stay prior to LT ≥ 7 d | 23 (71.9) | 216 (57.8) | 0.119 | |
Viral cirrhosis/necrosis/tumor | 21 (65.6) | 283 (75.7) | 0.209 | |
Alcoholic cirrhosis | 3 (9.4) | 28 (7.5) | 0.969 | |
Pre-LT diabetes | 7 (21.9) | 41 (11.0) | 0.067 | |
Pre-LT use of broad-spectrum antibiotics ≥ 3 d | 16 (50.0) | 150 (40.1) | 0.275 | |
Pre-LT creatinine ≥ 2 mg/dL | 1 (3.1) | 28 (7.5) | 0.574 | |
Infection within 2 months prior to LT | 17 (53.7) | 143 (38.2) | 0.098 | |
Pre-LT WBC count ≥ 10 × 109/L | 4 (12.5) | 55 (14.7) | 0.937 | |
Pre-LT lymphocyte count ≤ 0.5 × 109/L | 6 (18.8) | 92 (24.6) | 0.458 | |
Pre-LT platelet count ≤ 50 × 109/L | 12 (37.5) | 123 (32.9) | 0.595 | |
Pre-LT albumin level < 30 g/L | 9 (28.1) | 71 (19.0) | 0.212 | |
Donor age ≥ 50 yr | 13 (40.6) | 121 (32.4) | 0.340 | |
Steatosis ≥ 30% | 2 (6.3) | 40 (10.7) | 0.624 | |
Cold ischemia time ≥ 360 min | 15 (46.9) | 189 (50.5) | 0.691 | |
Duration of surgery ≥ 450 min | 10 (31.3) | 61 (16.3) | 0.033 | |
Intraoperative bleeding ≥ 3000 mL | 23 (71.9) | 214 (57.2) | 0.101 | |
Intraoperative RBC transfusion ≥ 12 U | 20 (62.5) | 201 (53.7) | 0.340 | |
ALT on day 1 after LT ≥ 1500U/L | 14 (43.8) | 66 (17.6) | <0.001 | |
Creatinine on day 3 after LT ≥ 2 mg/dL | 4 (12.5) | 57 (15.2) | 0.874 | |
Albumin level on day 1 after LT < 30 g/L | 4 (12.5) | 24 (6.4) | 0.347 | |
Post-LT duration of urethral catheter ≥ 4 d | 22 (68.8) | 167 (44.7) | 0.009 | |
Post-LT mechanical ventilation | 13 (40.6) | 81 (21.7) | 0.015 | |
Reoperation | 3 (9.4) | 14 (3.7) | 0.286 | |
Acute rejection | 6 (18.8) | 61 (16.3) | 0.721 | |
Post-LT renal replacement therapy | 3 (9.4) | 16 (4.3) | 0.382 | |
Glucocorticoidse ≥ 1500 mg | 21 (65.6) | 235 (62.8) | 0.754 | |
Basiliximab use ≥ 40 mg | 14 (43.8) | 145 (38.8) | 0.580 | |
Anti-thymocyte globulin use | 4 (12.5) | 14 (3.7) | 0.063 | |
Multivariate analysis | ||||
Female sex | 0.012 | 2.827 (1.256-6.364) | ||
Pre-LT diabetes | 0.036 | 2.794 (1.070-7.294) | ||
ALT on day 1 after LT ≥ 1500U/L | 0.001 | 3.645 (1.671-7.950) | ||
Post-LT duration of urethral catheter ≥ 4 d | 0.046 | 2.266 (1.016-5.054) |
Pearson’s chi-squared test was used to assess the effects of KPIs on the prognosis of LT recipients. Notably, patients with KPIs were more likely to have ICU stays of at least 7 d after LT than those without (56.3% vs 35.3%; P = 0.018). Patients with KPIs also had higher 6-month all-cause mortality than those without KPIs (17.6% vs 5.0%; P = 0.017). In contrast, patients with KPIs were not more likely to have post-LT hospitalization stays ≥ 21 d (P = 0.592) than those without (Table 5).
Variables | With infections caused by K. pneumoniae(32) | Without infections caused by K. pneumoniae (374) | χ2 | P value |
ICU stay after LT ≥ 7 d | 18 (56.3) | 132 (35.3) | 5.557 | 0.018 |
Hospitalization stay after LT ≥ 21 d | 26 (81.3) | 302 (80.7) | 0.288 | 0.592 |
All-cause mortality within 6 months after LT | 6 (18.8) | 32 (8.6) | 5.651 | 0.017 |
Univariate and multivariate analyses were performed to determine whether KPIs were independent risk factors for 6-month all-cause mortality. The multivariate analysis showed that KPIs were not a risk factor for 6-month all-cause mortality after LT. However, CRKP infections (OR = 5.330, 95%CI: 1.534-18.524; P = 0.008), female sex (OR = 2.829, 95%CI: 1.098-7.288; P = 0.031), intraoperative RBC transfusions ≥ 12 units (OR = 3.466, 95%CI: 1.259-9.543; P = 0.016), day 3 post-LT creatinine levels ≥ 2 mg/dL (OR = 9.724, 95%CI: 4.077-23.194; P < 0.001), and post-LT mechanical ventilation (OR = 4.118, 95%CI: 1.790-9.476; P = 0.001) were identified as risk factors for 6-month all-cause mortality after LT (Table 6).
Variables | Death(32) | Survival(374) | P value | OR (95%CI) |
Total | ||||
Univariate analysis | ||||
Female sex | 10 (31.3) | 62 (16.6) | 0.037 | |
Recipient age ≥ 55 yr | 14 (43.8) | 87 (23.3) | 0.010 | |
Recipient BMI ≥ 25 | 4 (12.5) | 102 (27.3) | 0.068 | |
MELD score at LT ≥ 22 | 24 (75.0) | 205 (54.8) | 0.027 | |
Hospital stay prior to LT ≥ 7 d | 24 (75.0) | 215 (57.5) | 0.053 | |
Viral cirrhosis/necrosis/tumor | 25 (78.1) | 279 (74.6) | 0.659 | |
Alcoholic cirrhosis | 1 (3.1) | 30 (8.0) | 0.513 | |
Pre-LT diabetes | 4 (12.5) | 44 (11.8) | 1.000 | |
Pre-LT creatinine ≥ 2 mg/dL | 6 (18.8) | 23 (6.1) | 0.008 | |
Infection within 2 months prior to LT | 19 (59.4) | 141 (37.7) | 0.016 | |
Pre-LT WBC count ≥ 10 × 109/L | 7 (21.9) | 52 (13.9) | 0.219 | |
Pre-LT lymphocyte count ≤ 0.5 × 109/L | 12 (37.5) | 86 (23.0) | 0.066 | |
Pre-LT platelet count ≤ 50 × 109/L | 8 (25.0) | 127 (34.0) | 0.302 | |
Pre-LT albumin level < 30g/L | 6 (18.8) | 74 (19.8) | 0.888 | |
Donor age ≥ 50 yr | 7 (21.9) | 127 (34.0) | 0.163 | |
Steatosis ≥ 30% | 3 (9.4) | 39 (10.4) | 1.000 | |
Cold ischemia time ≥ 360 min | 20 (62.5) | 199 (53.2) | 0.248 | |
Duration of surgery ≥ 450 min | 8 (25.0) | 63 (16.8) | 0.244 | |
Intraoperative bleeding ≥ 3000 mL | 26 (81.3) | 211 (56.4) | 0.006 | |
Intraoperative RBC transfusion ≥ 12 U | 25 (78.1) | 196 (52.4) | 0.005 | |
ALT on day 1 after LT ≥ 1500 U/L | 8 (25.0) | 72 (19.3) | 0.433 | |
Creatinine on day 3 after LT ≥ 2 mg/dL | 18 (56.3) | 43 (11.5) | < 0.001 | |
Albumin level on day 1 after LT < 30 g/L | 6 (18.8) | 25 (6.7) | 0.564 | |
Post-LT infections due to Klebsiella pneumoniae | 6 (18.8) | 26 (7.0) | 0.017 | |
Post-LT infections due to CRKP | 6 (18.8) | 15 (4.0) | < 0.001 | |
Post-LT mechanical ventilation | 19 (59.4) | 75 (20.1) | < 0.001 | |
Reoperation | 3 (9.4) | 14 (3.7) | 0.286 | |
Acute rejection | 4 (12.5) | 63 (16.8) | 0.525 | |
Post-LT renal replacement therapy | 8 (25.0) | 11 (2.9) | < 0.001 | |
Glucocorticoidse ≥ 1500 mg | 19 (59.4) | 237 (63.4) | 0.653 | |
Basiliximab use ≥ 40 mg | 10 (31.3) | 149 (39.8) | 0.339 | |
Anti-thymocyte globulin use | 1 (3.1) | 17 (4.5) | 1.000 | |
Multivariate analysis | ||||
Female sex | 0.031 | 2.829 (1.098-7.288) | ||
Intraoperative RBC transfusion ≥ 12 U | 0.016 | 3.466 (1.259-9.543) | ||
Creatinine on day 3 after LT ≥ 2 mg/dL | < 0.001 | 9.724 (4.077-23.194) | ||
Post-LT infections due to CRKP | 0.008 | 5.330 (1.534-18.524) | ||
Post-LT mechanical ventilation | 0.001 | 4.118 (1.790-9.476) |
Multivariate logistic regression analysis of factors related to prolonged ICU stays identified MELD scores ≥ 22 at LT (OR = 1.695, 95%CI: 1.086-2.645; P = 0.020), intraoperative blood loss ≥ 3000 mL (OR = 1.790, 95%CI: 1.139-2.813; P = 0.012), ALT levels ≥ 1500 U/L 1 d after LT (OR = 1.915, 95%CI: 1.123-3.265; P = 0.017), post-LT renal replacement therapy (OR = 4.058, 95%CI: 1.327-12.409; P = 0.014) and post-LT mechanical ventilation (OR = 3.402, 95%CI: 2.052-5.639; P < 0.001), but not KPIs or CRKP infections, as independent risk factors for post-LT ICU stays of at least 7 d (Table 7).
Variables | ICU stay after LT ≥ 7 d (150) | ICU stay after LT < 7 d (256) | P value | OR (95%CI) |
Total | ||||
Univariate analysis | ||||
Female sex | 34 (22.7) | 38 (14.8) | 0.046 | |
Recipient age ≥ 55 yr | 45 (30.0) | 56 (21.9) | 0.068 | |
Recipient BMI ≥ 25 | 38 (25.3) | 68 (26.6) | 0.785 | |
MELD score at LT ≥ 22 | 98 (65.3) | 131 (51.2) | 0.005 | |
Hospital stay prior to LT ≥ 7 d | 98 (65.3) | 141 (55.1) | 0.043 | |
Viral cirrhosis/necrosis/tumor | 112 (74.7) | 192 (75.0) | 0.940 | |
Alcoholic cirrhosis | 11 (7.3) | 20 (7.8) | 0.861 | |
Pre-LT diabetes | 17 (11.3) | 31 (12.1) | 0.815 | |
Pre-LT creatinine ≥ 2 mg/dL | 18 (12.0) | 11 (4.3) | 0.004 | |
Infection within 2 months prior to LT | 57 (38.0) | 103 (40.2) | 0.657 | |
Pre-LT WBC count ≥ 10 × 109/L | 27 (18.0) | 123 (48.0) | 0.129 | |
Pre-LT lymphocyte count ≤ 0.5 × 109/L | 34 (22.7) | 64 (25.0) | 0.596 | |
Pre-LT platelet count ≤ 50 × 109/L | 46 (30.7) | 89 (34.8) | 0.397 | |
Pre-LT albumin level < 30 g/L | 28 (18.7) | 123 (48.0) | 0.687 | |
Donor age ≥ 50 yr | 46 (30.7) | 88 (34.4) | 0.443 | |
Steatosis ≥ 30% | 16 (10.7) | 26 (10.2) | 0.871 | |
Cold ischemia time ≥ 360 min | 78 (52.0) | 136 (53.1) | 0.827 | |
Duration of surgery ≥ 450 min | 31 (20.7) | 40 (15.6) | 0.197 | |
Intraoperative bleeding ≥ 3000 ml | 102 (68.0) | 135 (52.7) | 0.003 | |
Intraoperative RBC transfusion ≥ 12 U | 92 (61.3) | 129 (50.4) | 0.033 | |
ALT on day 1 after LT ≥ 1500 U/L | 41 (27.3) | 39 (15.2) | 0.003 | |
Creatinine on day 3 after LT ≥ 2 mg/dL | 30 (20.0) | 31 (12.1) | 0.032 | |
Albumin level on day 1 after LT < 30 g/L | 12 (8.0) | 16 (6.3) | 0.502 | |
Post-LT infections due to Klebsiella pneumoniae | 18 (12.0) | 14 (5.5) | 0.018 | |
Post-LT infections due to CRKP | 15 (10.0) | 6 (2.3) | 0.001 | |
Post-LT mechanical ventilation | 59 (39.3) | 35 (13.7) | < 0.001 | |
Reoperation | 11 (7.3) | 6 (2.3) | 0.015 | |
Acute rejection | 28 (18.7) | 39 (15.2) | 0.369 | |
Post-LT renal replacement therapy | 14 (9.3) | 5 (2.0) | 0.001 | |
Glucocorticoidse ≥ 1500 mg | 102 (68.0) | 154 (60.2) | 0.114 | |
Basiliximab use ≥ 40 mg | 55 (36.7) | 104 (40.6) | 0.430 | |
Anti-thymocyte globulin use | 7 (4.7) | 11 (4.3) | 0.861 | |
Multivariate analysis | ||||
MELD score at LT ≥ 22 | 0.020 | 1.695 (1.086-2.645) | ||
Intraoperative bleeding ≥ 3000 ml | 0.012 | 1.790 (1.139-2.813) | ||
ALT on day 1 after LT ≥ 1500 U/L | 0.017 | 1.915 (1.123-3.265) | ||
Post-LT renal replacement therapy | 0.014 | 4.058 (1.327-12.409) | ||
Post-LT mechanical ventilation | < 0.001 | 3.402 (2.052-5.639) |
LT recipients are susceptible to opportunistic infections and antibiotic-resistant bacterial transmission due to malnutri
K. pneumoniae most commonly infects the bloodstream and urinary tract post-LT[6,15]. Pneumonia, tertiary peritonitis, and surgical site infections have been reported as complications of KPIs in LT recipients[8,15]. The present study found that the lung/thoracic cavity was the most frequent site of infection, followed by the bloodstream, abdominal/biliary tract, urinary tract, perianal region, and liver.
K. pneumoniae is a particularly concerning pathogen because it has limited antibiotic sensitivity and often develops multidrug resistance during treatment[16,17]. In our study, > 70% of the K. pneumoniae isolates were resistant to piperacillin/tazobactam, ceftazidime, cefepime, aztreonam, meropenem, or levofloxacin. The prevalence of CRKP infections was 5.2% in LT recipients, which is slightly lower than the rate of 7.0% reported in a previous study on LT recipients in China[1]. The rate of K. pneumoniae resistance to carbapenems reached 70.5%, which is similar to the rate of 63.3% re
Previous studies have demonstrated the following risk factors for CRKP infections in LT recipients: Colonization with CRKP, hepatocellular carcinoma, chronic kidney disease, preoperative infection, MELD score > 20, mechanical ven
Our analysis demonstrated that pre-LT diabetes is independently associated with the development of post-LT KPIs. The underlying mechanism may involve diabetes-induced immunosuppression. A previous study established a relationship between the risk factors of necrotizing soft tissue Klebsiella infections and diabetes mellitus[24]. Singh et al[25] revealed that diabetes mellitus is an independent and significant predictor of bacteremia in LT recipients.
We also revealed a post-LT urethral catheter duration of > 4 d to be an independent risk factor for post-LT KPIs. A uni
We identified female sex as a risk factor for KPIs, consistent with the findings of a study by Abbott et al[27], which claimed that females are more likely to be hospitalized for septicemia following kidney transplantation. In contrast, Bert et al[28] found male sex to be significantly associated with bloodstream infections post-LT. The most likely cause of the increased risk of KPIs in female LT recipients is their greater vulnerability to urinary tract infections. However, only 3 of the 44 K. pneumoniae strains in our study involved urinary tract infections. The reason for this is unclear, and therefore confirmation that the prolonged use of urethral catheters and female sex are independent risk factors for post-LT KPIs is required in further larger-sample studies.
Elevated post-LT ALT levels were also found to be an independent risk factor for post-LT KPIs. To the best of our knowledge, this is the first study to identify this risk factor, which resulted in a 3.6-fold increased risk of post-LT KPIs[28]. Higher ALT levels early after LT indicate severe intraoperative blood loss or hypotension or poor graft quality, all of which render LT recipients more susceptible to infection.
The present study revealed that KPIs have no impact on ICU or hospital stays or 6-month all-cause mortality rates. However, 6-month all-cause mortality is impacted by CRKP infections, in addition to female sex, intraoperative RBC transfusion, day 3 post-LT creatinine level, and post-LT mechanical ventilation. These results are consistent with those of a previous study that identified mechanical ventilation and CRKP infections as risk factors for three-month mortality after LT[1]. Previous studies have also shown that CRKP infections are independently associated with mortality rates in SOT recipients, which range from 40% to 75%[1,23,29,30].
This study has several limitations. First, the retrospective single-center design implies an inherent selection bias and represents only the regional prevalence of KPIs and CRKP infections in LT recipients. Second, many studies have stated that colonization with K. pneumoniae, particularly CRKP, prior to LT may be important for the risk of post-LT KPIs and CRKP infections. Unfortunately, surveillance for K. pneumoniae is not routinely performed at our center.
The homogeneity of infections caused by K. pneumoniae may lead to an accurate analysis of the risk factors for KPIs and mortality. Although our study included a relatively large cohort of LT recipients, the effect of KPIs, particularly CRKP infections, on patient outcomes emphasizes the need for further prospective studies. Given that the antimicrobial treatment of KPIs, especially CRKP infections, remains an ongoing challenge, knowledge of the risk factors for these infections and implementation of enhanced infection control measures are essential for successful LT.
Liver transplantation (LT) is the only curative treatment available for end-stage liver disease. However, LT recipients are prone to many types of infections, which are the most common cause of early mortality after LT. Recent studies have demonstrated that LT recipients suffer from bloodstream infections caused by K. pneumoniae. In addition, there has been little discussion on the adverse impacts of K. pneumoniae infections (KPIs) or carbapenem-resistant K. pneumoniae (CRKP) infections among LT recipients.
The key to retrospective cohort studies is to explore the risk factors for the development of KPIs in patients after LT and analyze drug resistance. Careful follow-up is required to minimize the occurrence of KPIs in patients with LT, reduce the development of drug resistance, and improve patient survival and prognosis.
The primary objective of this study was to assess the incidence, timing, distribution, drug resistance, and risk factors of KPIs within 3 months of LT. The secondary objective was to evaluate the impact of KPIs, particularly CRKP, on outcomes.
In total, 406 patients undergoing LT between January 2015 and January 2023 were included in the present retrospective study to investigate the risk factors for KPIs and assess the impact of KPIs and CRKP on the prognosis of LT recipients using logistic regression.
Of the 406 LT recipients recruited, 32 (7.9%) were infected with 44 strains of K. pneumoniae within 3 months post-LT. Of the 32 patients, 21 (65.6%) were infected with CRKP. The median time from LT to KPI onset was 7.5 d. KPIs (18.8%, 6/32) and CRKP infection (18.8%, 6/32) rates were significantly higher in patients who died than in those who survived (7.0%, 26/374 and 4.0%, 15/374, respectively). The multivariate analysis identified female sex [odds ratio (OR) = 2.827, 95% confidence interval (CI): 1.256-6.364, P = 0.012], pre-LT diabetes [OR = 2.794, 95%CI: 1.070-7.294, P = 0.036], day 1 post-LT alanine aminotransferase levels ≥ 1500 U/L (OR = 3.645, 95%CI: 1.671-7.950, P = 0.001), and post-LT urethral catheter durations > 4 d (OR = 2.266, 95%CI: 1.016-5.054, P = 0.046) were independently associated with the development of post-LT KPIs. On the prognosis of patients with LT, patients with KPIs were more likely to stay in the intensive care unit ≥ 7 d after LT than those without KPIs (56.3% vs 35.3%; P = 0.018). Patients with KPIs had a higher 6-month all-cause mortality rate than those without KPIs (17.6% vs 5.0%; P = 0.017). The multivariate analysis showed that KPIs were not risk factors for 6-month all-cause mortal
This novel retrospective assessment explored key factors in the prevention of KPIs or CRKP. Many risk factors play crucial roles in the development of KPIs after LT and in recipient prognosis. This study explored the role of KPIs in the prognosis of LT recipients and the risk factors for all KPIs after LT. By analyzing the distribution of KPIs and drug resistance, we demonstrated that risk factors are associated with surgical variables. Identifying these risk factors provides a basis for the prevention of KPIs, thereby improving the prognosis of LT recipients.
In future studies, we should obtain more data to more accurately identify other potential correlates of KPIs in patients with LT to reduce the occurrence of KPIs. In addition, monitoring K. pneumoniae, especially CRKP, colonization before LT may provide new insights.
We are grateful to all patients from whom we collected data, for their cooperation.
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Gastroenterology and hepatology
Country/Territory of origin: China
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P-Reviewer: Sivandzadeh GR, Iran S-Editor: Qu XL L-Editor: A P-Editor: Cai YX
1. | Liu N, Yang G, Dang Y, Liu X, Chen M, Dai F, Ding X, Li W, Li G, Lou J, Chen D, Yu Y. Epidemic, risk factors of carbapenem-resistant Klebsiella pneumoniae infection and its effect on the early prognosis of liver transplantation. Front Cell Infect Microbiol. 2022;12:976408. [PubMed] [DOI] [Cited in This Article: ] [Cited by in F6Publishing: 3] [Reference Citation Analysis (0)] |
2. | Kim WR, Lake JR, Smith JM, Skeans MA, Schladt DP, Edwards EB, Harper AM, Wainright JL, Snyder JJ, Israni AK, Kasiske BL. OPTN/SRTR 2013 Annual Data Report: liver. Am J Transplant. 2015;15 Suppl 2:1-28. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 245] [Cited by in F6Publishing: 242] [Article Influence: 26.9] [Reference Citation Analysis (0)] |
3. | Cervera C, van Delden C, Gavaldà J, Welte T, Akova M, Carratalà J; ESCMID Study Group for Infections in Compromised Hosts. Multidrug-resistant bacteria in solid organ transplant recipients. Clin Microbiol Infect. 2014;20 Suppl 7:49-73. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 100] [Cited by in F6Publishing: 110] [Article Influence: 11.0] [Reference Citation Analysis (0)] |
4. | Kim HK, Park YK, Wang HJ, Kim BW, Shin SY, Lim SK, Choi YH. Epidemiology and clinical features of post-transplant bloodstream infection: an analysis of 222 consecutive liver transplant recipients. Infect Chemother. 2013;45:315-324. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 31] [Cited by in F6Publishing: 39] [Article Influence: 3.5] [Reference Citation Analysis (0)] |
5. | Linares L, Cervera C, Hoyo I, Sanclemente G, Marco F, Cofán F, Ricart MJ, Navasa M, Moreno A. Klebsiella pneumoniae infection in solid organ transplant recipients: epidemiology and antibiotic resistance. Transplant Proc. 2010;42:2941-2943. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 56] [Cited by in F6Publishing: 59] [Article Influence: 4.5] [Reference Citation Analysis (0)] |
6. | Kalpoe JS, Sonnenberg E, Factor SH, del Rio Martin J, Schiano T, Patel G, Huprikar S. Mortality associated with carbapenem-resistant Klebsiella pneumoniae infections in liver transplant recipients. Liver Transpl. 2012;18:468-474. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 115] [Cited by in F6Publishing: 116] [Article Influence: 9.7] [Reference Citation Analysis (0)] |
7. | Bergamasco MD, Barroso Barbosa M, de Oliveira Garcia D, Cipullo R, Moreira JC, Baia C, Barbosa V, Abboud CS. Infection with Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae in solid organ transplantation. Transpl Infect Dis. 2012;14:198-205. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 122] [Cited by in F6Publishing: 119] [Article Influence: 9.2] [Reference Citation Analysis (0)] |
8. | Lübbert C, Becker-Rux D, Rodloff AC, Laudi S, Busch T, Bartels M, Kaisers UX. Colonization of liver transplant recipients with KPC-producing Klebsiella pneumoniae is associated with high infection rates and excess mortality: a case-control analysis. Infection. 2014;42:309-316. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 93] [Cited by in F6Publishing: 98] [Article Influence: 8.9] [Reference Citation Analysis (0)] |
9. | Lübbert C, Rodloff AC, Laudi S, Simon P, Busch T, Mössner J, Bartels M, Kaisers UX. Lessons learned from excess mortality associated with Klebsiella pneumoniae carbapenemase 2-producing K. pneumoniae in liver transplant recipients. Liver Transpl. 2014;20:736-738. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 12] [Cited by in F6Publishing: 18] [Article Influence: 1.8] [Reference Citation Analysis (0)] |
10. | Mouloudi E, Massa E, Piperidou M, Papadopoulos S, Iosifidis E, Roilides I, Theodoridou T, Kydona C, Fouzas I, Imvrios G, Papanikolaou V, Gritsi-Gerogianni N. Tigecycline for treatment of carbapenem-resistant Klebsiella pneumoniae infections after liver transplantation in the intensive care unit: a 3-year study. Transplant Proc. 2014;46:3219-3221. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 23] [Cited by in F6Publishing: 20] [Article Influence: 2.2] [Reference Citation Analysis (0)] |
11. | Pereira MR, Scully BF, Pouch SM, Uhlemann AC, Goudie S, Emond JE, Verna EC. Risk factors and outcomes of carbapenem-resistant Klebsiella pneumoniae infections in liver transplant recipients. Liver Transpl. 2015;21:1511-1519. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 65] [Cited by in F6Publishing: 71] [Article Influence: 7.9] [Reference Citation Analysis (0)] |
12. | Mouloudi E, Massa E, Papadopoulos S, Iosifidis E, Roilides I, Theodoridou T, Piperidou M, Orphanou A, Passakiotou M, Imvrios G, Fouzas I, Papanikolaou V, Gritsi-Gerogianni N. Bloodstream infections caused by carbapenemase-producing Klebsiella pneumoniae among intensive care unit patients after orthotopic liver transplantation: risk factors for infection and impact of resistance on outcomes. Transplant Proc. 2014;46:3216-3218. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 33] [Cited by in F6Publishing: 29] [Article Influence: 2.9] [Reference Citation Analysis (0)] |
13. | Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control. 2008;36:309-332. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 4031] [Cited by in F6Publishing: 4526] [Article Influence: 282.9] [Reference Citation Analysis (0)] |
14. | Wu D, Chen C, Liu T, Wan Q. Risk Factors for Acquisition of Carbapenem-Resistant Klebsiella pneumoniae and Mortality Among Abdominal Solid Organ Transplant Recipients with K. pneumoniae Infections. Med Sci Monit. 2020;26:e922996. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 2] [Cited by in F6Publishing: 4] [Article Influence: 1.0] [Reference Citation Analysis (0)] |
15. | Giannella M, Bartoletti M, Morelli MC, Tedeschi S, Cristini F, Tumietto F, Pasqualini E, Danese I, Campoli C, Lauria ND, Faenza S, Ercolani G, Lewis R, Pinna AD, Viale P. Risk factors for infection with carbapenem-resistant Klebsiella pneumoniae after liver transplantation: the importance of pre- and posttransplant colonization. Am J Transplant. 2015;15:1708-1715. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 87] [Cited by in F6Publishing: 88] [Article Influence: 9.8] [Reference Citation Analysis (0)] |
16. | Falagas ME, Lourida P, Poulikakos P, Rafailidis PI, Tansarli GS. Antibiotic treatment of infections due to carbapenem-resistant Enterobacteriaceae: systematic evaluation of the available evidence. Antimicrob Agents Chemother. 2014;58:654-663. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 246] [Cited by in F6Publishing: 256] [Article Influence: 23.3] [Reference Citation Analysis (0)] |
17. | Nordmann P, Cuzon G, Naas T. The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect Dis. 2009;9:228-236. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 1056] [Cited by in F6Publishing: 1092] [Article Influence: 72.8] [Reference Citation Analysis (0)] |
18. | Kohira N, West J, Ito A, Ito-Horiyama T, Nakamura R, Sato T, Rittenhouse S, Tsuji M, Yamano Y. In Vitro Antimicrobial Activity of a Siderophore Cephalosporin, S-649266, against Enterobacteriaceae Clinical Isolates, Including Carbapenem-Resistant Strains. Antimicrob Agents Chemother. 2016;60:729-734. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 188] [Cited by in F6Publishing: 181] [Article Influence: 22.6] [Reference Citation Analysis (0)] |
19. | Garonzik SM, Li J, Thamlikitkul V, Paterson DL, Shoham S, Jacob J, Silveira FP, Forrest A, Nation RL. Population pharmacokinetics of colistin methanesulfonate and formed colistin in critically ill patients from a multicenter study provide dosing suggestions for various categories of patients. Antimicrob Agents Chemother. 2011;55:3284-3294. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 537] [Cited by in F6Publishing: 547] [Article Influence: 42.1] [Reference Citation Analysis (0)] |
20. | van Duin D, Kaye KS, Neuner EA, Bonomo RA. Carbapenem-resistant Enterobacteriaceae: a review of treatment and outcomes. Diagn Microbiol Infect Dis. 2013;75:115-120. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 230] [Cited by in F6Publishing: 238] [Article Influence: 21.6] [Reference Citation Analysis (0)] |
21. | van Duin D, Lok JJ, Earley M, Cober E, Richter SS, Perez F, Salata RA, Kalayjian RC, Watkins RR, Doi Y, Kaye KS, Fowler VG Jr, Paterson DL, Bonomo RA, Evans S; Antibacterial Resistance Leadership Group. Colistin Versus Ceftazidime-Avibactam in the Treatment of Infections Due to Carbapenem-Resistant Enterobacteriaceae. Clin Infect Dis. 2018;66:163-171. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 344] [Cited by in F6Publishing: 437] [Article Influence: 87.4] [Reference Citation Analysis (0)] |
22. | Barchiesi F, Montalti R, Castelli P, Nicolini D, Staffolani S, Mocchegiani F, Fiorentini A, Manso E, Vivarelli M. Carbapenem-Resistant Klebsiella pneumoniae influences the outcome of early infections in liver transplant recipients. BMC Infect Dis. 2016;16:538. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 20] [Cited by in F6Publishing: 22] [Article Influence: 2.8] [Reference Citation Analysis (0)] |
23. | Bias TE, Malat GE, Lee DH, Sharma A, Doyle AM. Clinical outcomes associated with carbapenem resistant Klebsiella pneumoniae (CRKP) in abdominal solid organ transplant (SOT) recipients. Infect Dis (Lond). 2018;50:67-70. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 5] [Cited by in F6Publishing: 6] [Article Influence: 0.9] [Reference Citation Analysis (0)] |
24. | Ho PL, Tang WM, Yuen KY. Klebsiella pneumoniae necrotizing fasciitis associated with diabetes and liver cirrhosis. Clin Infect Dis. 2000;30:989-990. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 22] [Cited by in F6Publishing: 25] [Article Influence: 1.0] [Reference Citation Analysis (0)] |
25. | Singh N, Paterson DL, Gayowski T, Wagener MM, Marino IR. Predicting bacteremia and bacteremic mortality in liver transplant recipients. Liver Transpl. 2000;6:54-61. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 7] [Cited by in F6Publishing: 26] [Article Influence: 1.1] [Reference Citation Analysis (0)] |
26. | Zhang W, Wang W, Kang M, Wu S, Liu Y, Liao Q, Xiao Y, Ma Y, Xie Y. Bacterial and Fungal Infections After Liver Transplantation: Microbial Epidemiology, Risk Factors for Infection and Death with Infection. Ann Transplant. 2020;25:e921591. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 3] [Cited by in F6Publishing: 9] [Article Influence: 2.3] [Reference Citation Analysis (0)] |
27. | Abbott KC, Oliver JD 3rd, Hypolite I, Lepler LL, Kirk AD, Ko CW, Hawkes CA, Jones CA, Agodoa LY. Hospitalizations for bacterial septicemia after renal transplantation in the united states. Am J Nephrol. 2001;21:120-127. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 99] [Cited by in F6Publishing: 103] [Article Influence: 4.5] [Reference Citation Analysis (0)] |
28. | Bert F, Larroque B, Paugam-Burtz C, Janny S, Durand F, Dondero F, Valla DC, Belghiti J, Moreau R, Nicolas-Chanoine MH. Microbial epidemiology and outcome of bloodstream infections in liver transplant recipients: an analysis of 259 episodes. Liver Transpl. 2010;16:393-401. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 79] [Cited by in F6Publishing: 80] [Article Influence: 5.7] [Reference Citation Analysis (0)] |
29. | Wang Z, Qian Y, Bai H, Yang J, Li X. Allograft hemorrhage as a manifestation of carbapenem-resistant Klebsiella pneumonia infection in kidney transplant recipients: Case series. Medicine (Baltimore). 2020;99:e18982. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 5] [Cited by in F6Publishing: 5] [Article Influence: 1.3] [Reference Citation Analysis (0)] |
30. | Pagani N, Corcione S, Lupia T, Scabini S, Filippini C, Angilletta R, Shbaklo N, Mornese Pinna S, Romagnoli R, Biancone L, Cavallo R, Di Perri G, Solidoro P, Boffini M, De Rosa FG. Carbapenemase-Producing Klebsiella pneumoniae Colonization and Infection in Solid Organ Transplant Recipients: A Single-Center, Retrospective Study. Microorganisms. 2021;9. [PubMed] [DOI] [Cited in This Article: ] [Cited by in Crossref: 3] [Cited by in F6Publishing: 7] [Article Influence: 2.3] [Reference Citation Analysis (0)] |