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Saudi Journal of Kidney Diseases and Transplantation
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Table of Contents   
ORIGINAL ARTICLE  
Year : 2019  |  Volume : 30  |  Issue : 5  |  Page : 1065-1074
Long-term renal outcome and survival of kidney transplant recipients admitted to the intensive care unit


1 Department of Medicine, Faculty of Medicine and Medical Sciences, Arabian Gulf University; Nephrology Clinics, King Abdulla University Medical Center, Manama, Bahrain
2 Emergency Room Department, King Khalid Hospital, Alkharj, Saudi Arabia
3 Department of Nephrology, Salmaniya Medical Complex, Ministry of Health, Manama, Bahrain
4 Department of Immunology, Salmaniya Medical Complex, Ministry of Health, Manama, Bahrain

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Date of Submission16-Jul-2018
Date of Decision30-Jul-2018
Date of Acceptance01-Aug-2018
Date of Web Publication4-Nov-2019
 

   Abstract 


The goal of this study was to evaluate the course and outcome of kidney transplant (KT) recipients admitted to the intensive care unit (ICU). We reviewed the data of all adult renal transplant recipients who are admitted to the ICU at our center, between 1997 and 2017. Data reviewed included the demographic features, causes of end-stage renal disease, causes of admission, time between transplantation and admission, and ICU course and outcome. Among 379 KT recipients followed up in our center, 60 patients were admitted to the ICU and were categorized to early (during first 90 days; n = 28); intermediate (3–12 months; n = 7); and late (12 months and later, n = 25). The rate of ICU admission was 15.9%, and the mean age was 48.3 ± 12.6 years. The main reason for ICU admission was surgical complications (71%) in early group and infection (57% and 80%) in the intermediate and late groups, respectively. Mortality was significantly higher in late admission (52%) (P = 0.0001) and the leading cause of death in all groups was sepsis (89%). Twenty patients required ventilator that was an independent risk factor for mortality (P < 0.05). There was statistically significant decrease in the overall 5-year and 10-year patient survival (P = 0.031) in KT patients admitted to the ICU. The study shows that the main reason for ICU admissions was infections, especially in late admission. Mortality rate was relatively high and was linked to need for ventilator. Admission to the ICU is usually associated with decrease in the graft and patient survival.

How to cite this article:
El-Agroudy AE, Alqahtani AM, Dandi B, Farid E, Alaradhi A. Long-term renal outcome and survival of kidney transplant recipients admitted to the intensive care unit. Saudi J Kidney Dis Transpl 2019;30:1065-74

How to cite this URL:
El-Agroudy AE, Alqahtani AM, Dandi B, Farid E, Alaradhi A. Long-term renal outcome and survival of kidney transplant recipients admitted to the intensive care unit. Saudi J Kidney Dis Transpl [serial online] 2019 [cited 2019 Nov 20];30:1065-74. Available from: http://www.sjkdt.org/text.asp?2019/30/5/1065/270262



   Introduction Top


Kidney transplantation (KT) is the treatment of choice for most patients with end-stage renal disease (ESRD) and provides the highest survival benefit compared with other modalities of renal replacement therapy (RRT).[1]

KT recipients are at high risk for cardiovascular disorders, de novo malignancies, and infectious complications related to long-term exposure to induction and maintenance immunosuppressive therapy, which have become the leading causes of morbidity and mortality among such individuals.[2],[3] In addition, older patients with significant morbidity, who previously would not have been candidates for KT, are now considered as potential recipients.[4] Patients afflicted with such complications have been admitted to the intensive care unit (ICU), and carry mortality rates ranging between 16% and 59%.[4],[5],[6] Infectious complications (especially pneumonia) are the major cause of death.[7],[8],[9]

The reported incidence of admission of KT recipients to the ICU varies from 1% to 25%. This great discrepancy is probably because of the lack of uniformity of the criteria for ICU admission, which indeed are essentially center related.

Therefore, in the present study, we investigated the incidence, indications, clinical characteristics, and outcomes of patients admitted to the ICU and compared those patients with KT recipients not admitted to the ICU.


   Patients and Methods Top


This retrospective study was carried out at the Salmaniya Medical Complex in Manama, Bahrain, which is a 1200-bed hospital where an average of 20 KTs is performed each year. The hospital has an ICU with 30 beds. All consecutive renal transplant recipients admitted to our ICU from 1997 to January 2017 were included in this study. The reason for admission to ICU was classified into the following broad categories: cardiovascular, malignancy, cerebrovascular accident, infection, graft rejection, surgical complications, and miscellaneous. The Institutional Review Board approved the study and waived the need for informed consent.

We excluded patients younger than 16 years as well as those with burns or brain death. In case of multiple admissions to the ICU, during a single hospitalization, only the first admission to ICU was included.

Studied risk factors included patients’ age, gender, cause of ESRD, type of kidney donation, donor age, duration of RRT, immunosuppressive treatment, length of hospital stay, transplantation-admission interval (i.e., the time interval between the initial transplantation and the admission to ICU afterward) and mortality data, which were extracted from patients’ hospital records. In addition, data regarding ICU admission including the use of mechanical ventilation or dialysis, as well as the use of vasoactive drugs, during the ICU stay was extracted from the ICU charts.

Patients were separated into three groups to characterize the different indications and possible differences in outcomes. Group 1 comprised early ICU admissions within 90 days after transplantation, Group 2 comprised intermediate ICU admitted patients from three to 12 months after transplantation, and Group 3 comprised later admissions after one year of transplant.

To determine the risk factors of receiving intensive care, we compared ICU-admitted patients and other KT recipients not admitted to the ICU.

The initial immunosuppression protocol included an induction agent (basiliximab) with maintenance immunosuppression of a calcineurin inhibitor, cyclosporine and tacrolimus, an antimetabolite (mycophenolate mofetil), and steroids. Prophylaxis was used against Pneumocystis jiroveci and a Cytomegalovirus (CMV) prophylaxis was given during three months with ganciclovir and since 2005, valganciclovir.

Patients were followed up until the last follow-up or death, whichever occurred first.


   Statistical Analysis Top


We used the Statistical Package for the Social Sciences version 20.0 (IBM Corp., Armonk, NY, USA) for the statistical analysis. Continuous data were expressed as a mean ± standard deviation and compared using the Student’s t-test. Categorical data are expressed as percentage and compared using the Chi-square test and the Fisher’s exact test. All tests were two-tailed. For all comparisons, p <0.05 was considered significant. Survival analysis was performed through Kaplan–Meier method; and Log-rank was used to evaluate the differences among the groups. Factors associated with mortality were initially explored using univariate analysis and then factors that were significant were introduced in a multivariate logistic regression model to further explore significant associations. The following variables were introduced in the model: patients’ age, the type of donor and cause of ESRD, type of immunosuppression, reason for ICU admission, the need for ventilator, hemodialysis (HD), or vasopressors in the ICU.


   Results Top


During the study period, 118 (31.1%) KTs were performed at our facility and there were 261 (68.9%) KT recipients under long-term, post-transplantation follow-up (range, 1–6,845 days). Over this period, 60 KT recipients were admitted to the ICU. This cohort represented 15.9% of the total KTs followed-up over the same period. The mean age of the patients was 48.3 ± 12.6 years (range; 14 to 70 years); 40 (66.7%) were males. Most of the patients (50%) had received their transplants from a living-unrelated donor, while living-related and cadaver donors were the source of the trans-plant in 43% and 7%, respectively. The median time after transplantation to ICU admission was 4.4 months (range; 1–120). The characteristics of the KT recipients admitted to the ICU, is shown in [Table 1].
Table 1: Pretransplant variables in intensive care unit kidney transplant patients.

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Twelve patients (21.1%) were admitted to the ICU less than one month after KT. Diagnoses on admission to the ICU are listed in [Table 2]. The ICU admissions were frequently motivated by an infectious disease, 37 patients (61.7%) presenting with this diagnosis, particularly of pulmonary origin. CMV status in either the donor or recipient was negative in all patient populations. Fourteen of these patients were in septic shock. Twenty patients (33.3%) were admitted due to surgical causes mainly postoperative, three patients (5%) following cardiac events, 1.6% for GI bleeding and hepatic encephalopathy each and 3.33% with established severe respiratory airway obstruction.
Table 2: Pre- and post-transplant variables in the three groups of intensive care unit admitted patients.

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We categorized the admitted patients to ICU according to the time post-transplant into three groups: early, intermediate, and late. Most of the early group (17 patients; 61%) were transplanted outside Bahrain from unrelated donor. We did not find any significant differences between groups regarding recipient age and gender; donor type (living or deceased), presence of pre-transplant morbidities such as hypertension, hepatitis, or duration of pre-transplant dialysis as shown in [Table 1] and [Table 2].

Reasons for ICU admission of the renal transplant recipients were statistically different between the three groups (P = 0.001). In the early group, the major reason for elective admission of patients to the ICU was preemptive in patients with pre-transplant cardiac and respiratory impairment. Causes of admission in this group included postoperative surgical complications and care (71%); they included lymphocele (5 patients), wound dehiscence (3 patients), urinoma (2 patients), and urinary leakage (3 patients). Four of the patients in this group were admitted after surgery unrelated to KT (two after an operation for peripheral vascular disease and two after a laparotomy for intestinal obstruction). We found infections in eight patients due to wound infection (5 patients) and pneumonia (3 patients). Among the intermediate group, four patients (57%) were admitted to the ICU due to respiratory tract bacterial infectious complications, two due to cardiovascular complications (one myocardial infarction and one arrhythmia) and one due to cerebral stroke. In the late group, infections were the most common indications for admission (18/25, 72%). Bacterial pneumonia was the most common infection (14 patients), followed by urinary tract infection in three patients and tuberculosis in one patient [Table 3]. Five of 18 patients with documented infections developed severe sepsis shortly after ICU admission (sepsis plus organ dysfunction). Two patients had severe sepsis at the time of admission. Two patients in this group were admitted with severe bronchial asthma, one with massive gastrointestinal bleeding due to peptic ulcer, one with hepatic encephalopathy and one with shock due to severe diarrhea.
Table 3: Course of intensive care unit kidney transplant patients.

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Course in the intensive care unit

Most patients in the late group (60%) and intermediate group (43%) required mechanical ventilation which was significantly different between groups (P = 0.001), and the need for mechanical ventilation for any reason was associated with a worse outcome with only 34% of those ventilated surviving to hospital discharge compared to 66% in patients not requiring mechanical ventilation (P = 0.043). A minority of patients required renal replacement therapy (12% in late group; P = 0.056); however, the need for inotropic support (0%, 14%; and 11% in early, intermediate, and late groups, respectively) was comparable (P = 0.067). The median ICU stay was five days (range; 1–102 days). The late group tended to have a longer ICU stay than other groups as shown in [Table 3] (median: 2.5, 7, and 10 days in early, intermediate, and late groups, respectively) ; however, the length of stay in the ICU was not significantly different between groups (P = 0.183).

Long-term mortality of ICU admitted patients

The mortality rate of the study group was 55% (33 patients), 18 (30%) died in the ICU, and nine (15%) died within the first 90 days after being discharged from the ICU, while six (10%) died later on.

Mortality of admitted patients on discharge from intensive care unit

Causes of mortality on discharge are shown in [Table 3]. Eleven patients died of septic shock; hence, the infection was the most common reason of ICU admission. Hepatic encephalo-pathy and myocardial infarction were responsible for mortality in the other two patients. The need for mechanical ventilation (P = 0.015), hemodynamic support (P = 0.046), and longer duration of stay in the ICU (P = 0.038) were found to be significant predictors of mortality on univariate analysis. On multivariate analysis, the need for mechanical ventilation was the only independent risk factor for mortality on discharge. On multivariate analysis, the following variables were introduced in the model: patient age, need for HD in the ICU, cause of admission, length of ICU stay, the type of donor and cause of ESRD.

Long-term graft outcome and survival

[Table 4] shows the long-term clinical outcome and clinical grading of functioning grafts at last follow-up of the three groups. There was a statistically significant increased graft loss in patients admitted to the ICU (P = 0.022). Only five patients (20%) from the late group and 15 patients (54%) from the early group still had functioning graft at last follow-up. Most of these patients had graft function with serum creatinine >140 μmol/L. Death with functioning graft was the predominant cause of graft loss in surviving ICU patients in all groups, which resulted in nearly 62% of lost grafts in early group and 57% and 55% in intermediate and late groups, respectively. Other main causes of graft loss included chronic rejection (31%, 29%, and 40%) and acute rejection (8%, 14%, and 5%) in the three groups, respectively. The causes of graft loss were not significantly different between the three groups (P = 0.058).
Table 4: Outcome of intensive care unit kidney transplant patients.

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When we compared KT recipients admitted to the ICU with matched KT recipients not admitted to the ICU, there was statistically significant decrease in the overall 5-year and 10-year patient survival (P = 0.031, 95% confidence interval = 9.8–14.1) in KT patients admitted to the ICU (70% and 62%) when compared with patients not admitted to the ICU (88.5% and 78%) as shown in [Figure 1].
Figure 1: Kaplan–Meier Patient Survival Curve of ICU admitted and non-admitted kidney transplant patients.
ICU: Intensive care unit.


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Overall, death with functioning graft accounted for 38% of all graft losses in the patients admitted to the ICU, while it was 13% in patients not admitted to the ICU (P = 0.015) as shown in [Table 5]. Almost two-thirds (67%) of patients died due to infectious complications and cardiovascular disease was responsible for death in 21% in the ICU admitted patients, while it was 55% and 25% in the KTs not admitted to the ICU. These results were statistically significant (P = 0.049).
Table 5: Outcome of intensive care unit and non-intensive care unit transplant patients.

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   Discussion Top


KT has become the treatment of choice for ESRD.[1] These patients carry a high risk of multi-organ dysfunction due mainly to preexistent medical problems and to chronic immunosuppression. Severe transplant-related complications require ICU admission.[4],[5],[6],[7]

The goal of this article was to evaluate the course and long-term outcome of renal transplant recipients admitted to the ICU. In our study, 15.9% of renal transplant recipients were admitted to the ICU. ICU admission rate in our patients was in agreement with rates reported in many previous studies. In a singlecenter study, the ICU admission rate was 6.4%,[11] and other studies have found rates of up to 41%.[4],[5],[6] These differences may be related to many factors, since admission policies vary widely across centers with great differences in medical complications needed to be admitted to the ICU.[16] The study of Sadaghdar et al,[4] reported a high rate of ICU admission, where they found among 178 KT performed during their one-year study period, 41.6% were admitted to the ICU. However, three more recent studies reported far lower use of ICU in this setting. In 2011, in a large observational study carried out in nine high-volume transplant centers in France over an eight-year study period, they found that 6.6% of KT recipients required ICU admission.[17] Our results show that most of our ICU admissions occur in the late posttransplant period (≥6 months). In the study by Bige et al,[18] median time from transplantation to ICU admission was 21.9 months and 17 months in the study by Canet et al.[17]

Causes of post-KT ICU admission depend on the interval between transplantation and admission. In our study, the early group of patients who constituted 47% of our study patients admitted to the ICU, principally as a pre-emptive measure for monitoring with a short ICU stay. The inter-mediate and late groups constituted 53% of patients admitted to the ICU, and infection was consistently the leading reason for ICU admission (75%). A study conducted in Australia reported that 59% of KT experienced at least one surgical, urological, or wound complication. However, only 6% required ICU admission.[18] These complications usually occur in the first month posttransplantation and portends a good prognosis.[16] Technical problems, such as improper suturing technique, compression by hematomas or lymphoceles seemed to be more prevalent in patients who underwent KT from unrelated donor outside Bahrain and these complications seem preventable with a better care.

In our study, the lung was the most common site of infection, which is in agreement with other sepsis cohort studies.[9],[12],[13],[15],[17] The risk of infection in these patients is well recognized and it is determined primarily by the magnitude of exposure to pathogens and by the level of immunosuppression.[17] This finding was expected, since respiratory infection is the leading cause of ICU admission and acute respiratory failure in KT recipients.[11],[13],[15],[17] Candan et al[9] reported that infection-related and respiratory problems were the most common indications for late ICU admissions, with an incidence of 61.5% during a four-year follow-up period. In our study, we did not see any cases with viral pneumonia. CMV was historically the leading virus identified in the severe forms of pneumonia.[19] In the current era, with the prophylaxis and pre-emptive treatment strategies, CMV pneumonia is much less common. In a study conducted in Finland and Germany among 1129 KT screened over an eight-year period, CMV pneumonia was confirmed in only three patients. [20],[21]

KT present risk for the development of cardiovascular diseases, which are frequent CO-morbidities and are the main cause of morbidity and mortality in this population.[1],[22] Although it is reported as being frequently responsible for ICU admission, only eight of our patients were admitted to ICU for this reason. We found that gastrointestinal bleeding and hepatitis were responsible for 5% of ICU admissions. Increased risk of gastrointestinal bleeding and hepatitis has been reported.[3],[23] Immunosuppressive drugs not only increase the risk of infections but their side effects also add to the risk of multi-organ dysfunction.[23]

In our study, among the patients admitted to ICU, one-third required mechanical ventilation and nearly 13% required vasopressor support during their stay in the ICU. Most of these patients were due to respiratory failure in the late group as shown in [Table 3]. Our results are in accordance with previous reports.[4],[8],[16] However, this rate was higher (more than half of the patients) in the study of Kirilov et al.[5] It was not surprising that patients with respiretory problems needed more mechanical ventilation support compared with patients with no respiratory problems. During the ICU stay, about 5% of the recipients required HD. This rate is in line with 5%–10% reported in critically ill patients.[24] Indeed, KT are at high-risk for acute kidney injury throughout the ICU stay. In addition to several exposure factors (sepsis, shock, nephrotoxic drugs, radiocontrast agents), an impaired baseline graft function before ICU admission is detrimental.[23],[24]

The hospital mortality rate for ICU KT recipients varies greatly in the literature, and this may be ascribed to differences in the study periods and in ICU admission policies.[14] In our study, the overall ICU mortality rate was 33%. These numbers are in line with the study of Kirilov et al[5] who reported the mortality rate to be 32.4% and Nicolet et al,[8] who reported the mortality rates to be 33% and higher than 16% reported by Sadaghdar et al,[4] but differs from higher rates reported elsewhere.[7],[11],[12],[16] However, these results should be interpreted cautiously, taking into account the degree of severity of the patients admitted to an ICU in each individual study. The lower reported ICU mortality rate (16%) reported by Sadaghdar et al,[4] may be explained by the fewer patients who had respiratory problems and admission criteria to the ICU may have been different than our ICU admission criteria. Factors reported to be independently associated with mortality in critically ill kidney recipients are sepsis, mechanical ventilation, the number of organ dysfunctions, acute physiology and chronic health evaluation score and long ICU stay.[8],[11],[16],[18] Our results showed that only ventilation support was statistically significant as a positive predictor of mortality that was similar to the study of Nicolet et al,[8] who associated the mortality rate with mechanical ventilation and Klouche et al[11] who found that the need for catecholamine support, mechanical ventilation or dialysis during the ICU stay worsened the outcome significantly. None of the transplant-related characteristics had been reported to be associated with ICU or hospital mortality as in line with our results.[10],[11],[16],[18],[21]

The deleterious impact of ICU admission on long-term graft survival and patient survival also deserves attention. When compared to KT patients not admitted to ICU, we found that ICU admission worsened the graft and patient survival in our study. Our study reported a 10-year patient survival of 62% in ICU admitted patients compared with 78% in kidney transplants not admitted to ICU (P = 0.031). Nearly 67% lost their graft and 57% out of them due to death with function graft as shown in [Table 5]. The lack of similar studies in literature precluded a comparison of our experience with that of others. The impact on long-term patient survival has been poorly studied. Only, Shorr et al[25] demonstrated that the three-year survival after KT in individuals who had acute respiratory distress syndrome was 57.8% as compared with 88.9% in those who did not. In another study by Arulkumaran et al,[13] they found from the time of hospital discharge, 26% died over a three-year follow-up. We found that patients in the early admission group, had a better long-term graft outcome than those admitted later (54% versus 0% and 20% in later groups). Factors that may contribute to explaining graft loss include bacterial infection with septic shock.

Our study has some potential limitations. First, it was a retrospective study that can be affected by various bias. Second, it is a single center study with a relatively small sample size, which limits the reproducibility of our findings. Third, we included patients over a long period during which changes in treatment practices probably occurred. Fourth, our study lacks information on several factors that might influence prognosis, such as the degree of acute physiological disturbance and the use of other ICU procedures.


   Conclusions Top


Posttransplant complications requiring ICU admission occurred in 15.9% of transplant recipients, and infection accounted for more than one-half of these admissions. Whereas patients admitted in the immediate postoperative period usually had a shorter ICU stay, the later groups had a relatively longer stay, requiring more intensive and invasive ICU care and consequently were more susceptible to ICU-related complications. Mortality was significantly higher for later ICU admissions and was predominantly related to sepsis and use of ventilators. Long-term graft and patient survival was less than kidney transplant patients not admitted to the ICU and most of the patients admitted to the ICU died with functioning graft due to sepsis.



 
   References Top

1.
Suthanthiran M, Strom TB. Renal transplantation. N Engl J Med 1994;331:365-76.  Back to cited text no. 1
    
2.
Hariharan S, Johnson CP, Bresnahan BA, Taranto SE, McIntosh MJ, Stablein D. Improved graft survival after renal transplantation in the United States, 1988 to 1996. N Engl J Med 2000:342:605-12.  Back to cited text no. 2
    
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Ramanathan V, Goral s, Helderman JH. Renal transplantation. Semin Nephrol 2001:21:213-9.  Back to cited text no. 3
    
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Sadaghdar H, Chelluri L, Bowles SA, Shapiro R. Outcome of renal transplant recipients in the ICU. Chest 1995:107:1402-5.  Back to cited text no. 4
    
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Kirilov D, Cohen J, Shapiro M, Grozovski E, Singer P. The course and outcome of renal transplant recipients admitted to a general intensive care unit. Transplant Proc 2003:35: 606.  Back to cited text no. 5
    
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Kogan A, Singer P, Cohen J, et al. Readmission to an intensive care unit following liver and kidney transplantation: A 50-month study. Transplant Proc 1999:31: 1892-3.  Back to cited text no. 6
    
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Scroggs MW, Wolfe JA, Bollinger RR, Sanfilippo F. Causes of death in renal transplant recipients. A review of autopsy findings from 1966 through 1985. Arch Pathol Lab Med 1987:111:983-7.  Back to cited text no. 7
    
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Nicolet L, Heng AE, Souweine B, et al. Outcome of renal transplant recipients and graft survival in the ICU. Crit Care 2001:5 Suppl 1:221-3.  Back to cited text no. 8
    
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Candan S, Pirat A, Varol G, Torgay A, Zeyneloglu P, Arslan G. Respiratory problems in renal transplant recipients admitted to intensive care during long-term follow-up. Transplant Proc 2006:38:1354-6.  Back to cited text no. 9
    
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Mouloudi E, Massa E, Georgiadou E, et al. Course and outcome of renal transplant recipients admitted to the intensive care unit: A 20-year study. Transplant Proc 2012:44:2718-20.  Back to cited text no. 10
    
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Klouche K, Amigues L, Massanet p, et al. Outcome of renal transplant recipients admitted to an intensive care unit: A 10-year cohort study. Transplantation 2009:87:889-95.  Back to cited text no. 11
    
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Aldawood A. The course and outcome of renal transplant recipients admitted to the intensive care unit at a tertiary hospital in Saudi Arabia. Saudi J Kidney Dis Transpl 2007:18:536-40.  Back to cited text no. 12
    
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Arulkumaran N, West S, Chan K, Templeton M, Taube D, Brett SJ. Long-term renal function and survival of renal transplant recipients admitted to the intensive care unit. Clin Transplant 2012;26:E24-31.  Back to cited text no. 13
    
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Marques ID, Caires RA, Machado DJ, Goldenstein PT, Rodrigues CE, Pegas JC, et al. Outcomes and mortality in renal transplant recipients admitted to the intensive care unit. Transplant Proc 2015;47:2694-9.  Back to cited text no. 14
    
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Veroux M, Giuffrida G, Corona D, et al. Infective complications in renal allograft recipients: Epidemiology and outcome. Transplant Proc 2008;40:1873-6.  Back to cited text no. 15
    
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Canet E, Zafrani L, Azoulay É. The critically ill kidney transplant recipient: A Narrative review. Chest 2016:149:1546-55.  Back to cited text no. 16
    
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Canet E, Osman D, Lambert J, et al. Acute respiratory failure in kidney transplant recipients: A multicenter study. Crit Care 2011;15:R91.  Back to cited text no. 17
    
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Bige N, Zafrani L, Lambert J, et al. Severe infections requiring intensive care unit admission in kidney transplant recipients: Impact on graft outcome. Transpl Infect Dis 2014:16:588-96.  Back to cited text no. 18
    
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Patel R, Paya CV. Infections in solid-organ transplant recipients. Clin Microbiol Rev 1997:10:86-124.  Back to cited text no. 19
    
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Sawyer RG, Crabtree TD, Gleason TG, Antevil JL, Pruett TL. Impact of solid organ transplantation and immunosuppression on fever, leukocytosis, and physiologic response during bacterial and fungal infections. Clin Transplant 1999;13:260-5.  Back to cited text no. 20
    
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de Carvalho MA, Freitas FG, Silva Junior HT, et al. Mortality predictors in renal transplant recipients with severe sepsis and septic shock. PLoS One 2014;9:e111610.  Back to cited text no. 21
    
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Silva RM, Freitas FG, Bafi AT, Silva Junior HT, Roza BA. Factors associated with hospital mortality in renal transplant patients admitted to the intensive care unit with acute respiratory failure. J Bras Nephrol 2017:39:433-40.  Back to cited text no. 22
    
23.
Lak M, Jalali AR, Badrkhahan SF, et al. Additional burden of intensive care to rehospitalizations following kidney transplantation: A study of rate, causes, and risk factors. Iran J Kidney Dis 2008;2:212-7.  Back to cited text no. 23
    
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Uchino S, Kellum JA, Bellomo R, et al. Acute renal failure in critically ill patients: A multinational, multicenter study. JAMA 2005;294:813-8.  Back to cited text no. 24
    
25.
Shorr AF, Abbott KC, Agadoa LY. Acute respiratory distress syndrome after kidney transplantation: Epidemiology, risk factors, and outcomes. Crit Care Med 2003:31:1325-30.  Back to cited text no. 25
    

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Correspondence Address:
Amgad E El-Agroudy
Department of Medicine, Faculty of Medicine and Medical Sciences, Arabian Gulf University, Manama
Bahrain
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DOI: 10.4103/1319-2442.270262

PMID: 31696845

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