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Saudi Journal of Kidney Diseases and Transplantation
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Year : 2013  |  Volume : 24  |  Issue : 3  |  Page : 620-629
Renal involvement in sepsis: A prospective single-center study of 136 cases

1 Department of Nephrology and Clinical Transplantation, Institute of Kidney Diseases and Research Center and Dr. H. L. Trivedi Institute of Transplantation Sciences (IKDRC-ITS), Civil Hospital Campus, Asarwa, Ahmedabad, India
2 Department of Pathology, Laboratory Medicine, Transfusion Services and Immunohematology, Institute of Kidney Diseases and Research Center and Dr. H. L. Trivedi Institute of Transplantation Sciences (IKDRC-ITS), Civil Hospital Campus, Asarwa, Ahmedabad, Gujarat, India

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Date of Web Publication24-Apr-2013


Acute kidney injury (AKI) is an independent risk factor for mortality in sepsis syndrome. Few Indian studies have focused on describing the epidemiology of sepsis with AKI. Adult patients with sepsis-induced AKI were evaluated for the clinical characteristics and outcome and to correlate various parameters associated with sepsis to the outcome of patients. This prospective study included 136 patients with sepsis-induced AKI between 2007 and 2009. All patients required renal replacement therapy. Males comprised 44% of the patients while 56% were females; their mean age was 38.6 years. When we compared the survivor and non-survivor groups, it was found that mortality was associated with delayed presentation (6.8 vs 9.4 days), presence of hypotension (132/80 vs 112/70 mmHg), oliguria (300 vs 130 mL), anemia (8 vs 9.3 gm/dL), prolonged prothrombin time (15 vs 29 s) and activated partial thrombin time (38 vs 46 s), creatinine (7.8 vs 6.4 mg/dL), blood urea (161 vs 135 mg/dL), higher D-dimer (1603 vs 2185), short hospital stay (27.9 vs 8.3 days), number of hemodialysis sessions (11.9 vs 6 times), need for vasopressors (14% vs 52%) and ventilator (7.2% vs 75%) and higher Sequential Organ Failure Assessment (SOFA) score (6.7 vs 11.4) (P <0.05). The most com­mon source of infection in this study was urogenital tract (34%). About 51.4% showed complete recovery of renal function. The overall hospital mortality rate was 38.9%. Less than 10% of the pa­tients developed impaired renal function following septic AKI. In conclusion, the most common renal manifestation of sepsis was AKI, which is a risk factor for mortality in sepsis syndrome. SOFA score >11 and multi-organ dysfunction are the risk factors for mortality.

How to cite this article:
Shah PR, Gireesh M S, Kute VB, Vanikar AV, Gumber MR, Patel HV, Goplani K R, Trivedi HL. Renal involvement in sepsis: A prospective single-center study of 136 cases. Saudi J Kidney Dis Transpl 2013;24:620-9

How to cite this URL:
Shah PR, Gireesh M S, Kute VB, Vanikar AV, Gumber MR, Patel HV, Goplani K R, Trivedi HL. Renal involvement in sepsis: A prospective single-center study of 136 cases. Saudi J Kidney Dis Transpl [serial online] 2013 [cited 2022 Nov 28];24:620-9. Available from: https://www.sjkdt.org/text.asp?2013/24/3/620/111089

   Introduction Top

Among the several disorders encountered in sepsis, acute kidney injury (AKI) is one of the most important because it is a life-threatening condition, it increases the complexity and cost of care and is an independent risk factor for mortality. [1],[2] The most common renal manifestation of infection is AKI. The incidence of sepsis-related hospital admissions appears to be rising and increasing in parallel to the incidence of sepsis, the incidence of AKI is increasing. [1],[2],[4],[5],[6] Although recent advances in critical care management have improved the overall survival in the intensive care unit (ICU), the same cannot be said for the criti­cally ill with AKI. [3],[7] Even in patients not re­quiring dialysis, AKI is shown to worsen prog­nosis in critical illness and, when dialysis is required, the ICU mortality rises from 45% to 80%. [1],[8],[9] Relatively few studies have focused on describing the epidemiology of sepsis-related AKI, [10] and still less from the Indian sub­continent. This study was undertaken to eva­luate the occurrence, risk factors and outcome of patients with renal involvement in sepsis.

   Materials and Methods Top

This prospective study was performed to eva­luate the clinical characteristics of adult pa­tients with sepsis-induced AKI, to describe its clinical outcomes and to correlate the various parameters associated with sepsis to the out­come of patients. The study population inclu­ded all patients aged >12 years and diagnosed to have sepsis with AKI admitted between November 2007 and October 2009. They were further followed for six more months till April 2010. Only those patients with no prior under­lying renal disease were included in the study.

The inclusion criteria were age >12 years, fulfillment of at least two criteria for systemic inflammation, proven or suspected infection and diagnosed to have AKI. Exclusion criteria were age ≤12 years, chronic renal impairment, history of diabetes mellitus or hypertension, nephrotic syndrome and any other type of renal involvement where chronic injury is a possibility (like renal stone disease, single kidney, immune disorders of kidney, heredi­tary renal diseases, renal transplant recipients, history of AKI in the past from which the pa­tient would have apparently recovered, sus­pected or proven fungal infection and patients who were on immunosuppressive therapy).

The criteria used for the diagnosis of sepsis were according to the 2001 International Sep­sis Definitions Conference. The operational definition and criteria for AKI were presence of at least one of the following: (a) oliguria, defined as urine output <200 mL over 12 h, (b) azotemia, defined as serum creatinine (SCr) >1.5 mg/dL and (c) need for acute renal re­placement therapy. A septic origin of AKI was diagnosed in any AKI patient with a recog­nized source of infection, whether blood cultures were positive or not.

Data collection was as per the proforma that included age, sex, detailed history, clinical exa­mination, radiological evaluation, laboratory investigations and review of previous medical records. The SCr and urine output values were used to calculate the RIFLE (R for risk, I for injury, F for failure, L for loss, and E for end-stage) score. Physiological, hematological and biochemical variables were measured at ad­mission in order to calculate the Sequential Organ Failure Assessment (SOFA) score and to define the severity of disease.

The patients were treated with appropriate antibiotics and other supportive measures as required. They received hemodialysis (HD) on alternate days till required as determined by their SCr, urine output, fluid status, acidosis, serum potassium levels, etc. HD was initiated and continued if SCr was ≥4 mg% and/or urine output was less than 400 mL/24 h and/or the patient had acidosis, hyperkalemia or fluid overload not responding to conservative ma­nagement. Few patients received daily or more than one HD session per day when required due to their fluid overload or metabolic status. HD was administered as 3-4 h sessions of stan­dard bicarbonate dialysis. Patients whose hemo­dynamic status was unstable received sus­tained low-efficiency dialysis (SLED) till he­modynamic stability was achieved. The SCr of the study patients at discharge and on follow-up till six months was noted.

All the biochemical investigations were per­formed using a fully automated analyzer (Dade Behring Dimension RLMax) using a Flex rea­gent cartridge (Flex reagent cartridge, Siemens, Newark, USA). D-dimer assay was performed by immuno-turbidometric assay using kits by Diagnostica Stago (STA Liatest D-DI, Diagnostica Stago S.A.S, France). Procalcitonin (PCT), as a marker of sepsis, was tested by Lumino immuno assay on a Lumitest Proca-S (BRAHMS- Diagnostica, Berlin, Germany). D-dimer and PCT were tested in 129 and 55 patients, respectively, due to financial constrains.

Outcomes were based on S Cr at six months after discharge. Outcomes were recorded as complete recovery [SCr in the normal range (<1.5 mg/dL)], partial recovery [SCr above normal range but dialysis independent (≥1.5 mg/dL and <6 mg /dL)], end-stage renal di­sease (ESRD) (SCr ≥6 mg/dL or dialysis de­pendent) or death (expired during the hospital stay).

A total of 140 patients were included in the study, of whom 83 patients survived and 53 patients expired. Four patients had taken dis­charge against medical advice and, hence, were excluded from the analysis. The charac­teristics of the remaining 136 patients are des­cribed below. Permission for the study was obtained from the institutional ethics commi­ttee. Informed consent was taken from the patients or their relatives.

   Statistical Analysis Top

Analysis was performed using SPSS version 15. Normally or near normally distributed va­riables are presented as means and SD and compared using the t test. Categorical varia­bles were compared using the chi square test.

Z-test was used for comparison of proportions. Pearson's correlation coefficient was used for calculating correlation. A P-value of <0.05 was considered statistically significant.

   Results Top

The mean age of the study patients was 38.4 ± 15.9 years. There was no significant diffe­rence between the mean age of survivors and non-survivors. The maximum number of pa­tients was from the younger age-group, i.e. 12-30 years. It was seen that patients above the age of 50 years were more common in the non-survivor group (32.1%) than in the sur­vivor group (18.1%). Sex distribution revealed a female preponderance, with 55.9% of the total patients being female. The same pattern was seen in both the survivors and the non-survivors. Clinical profile and hematological/ biochemical parameters in survivors and non-survivors are shown in [Table 1] and [Table 2]. Ana­lysis of serum bilirubin and serum glutamate pyruvate transaminase (SGPT) values showed that almost two-thirds of the survivors (64.9%) had serum bilirubin values of ≤1.5 mg%, whereas two-thirds of the non-survivors (66%) had an elevated value of >1.5 mg%. With SGPT, it was seen that a higher proportion of non-survivors (60.3%) had elevated values of values of >40 U/L.
Table 1: Clinical profile among survivors and non-survivors.

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Table 2: Laboratory parameters among survivors and non-survivors.

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There was a significant difference in D-dimer values between the two groups, with levels being lower in survivors as compared with non-survivors; however, the difference in mean value between the two groups was insignificant with respect to PCT [Table 3]. Considering D-dimer levels <500 ng/mL as normal, most of the patients (~76%) were found to have ab­normal levels.
Table 3: Tests for sepsis among survivors and non-survivors.

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PCT levels were high in all patients when the cut-off was taken at 0.25 ng/mL. The least va­lue observed was 0.27 ng/mL and the highest value observed was 293.32 ng/mL. When a higher cut-off of 2 ng/mL was considered to be indicative of severe sepsis, only six patients (10.9%) were found to have a value less than 2 ng/mL. All these six patients survived. None of the patients in the non-survivor group had a PCT less than 2 ng/mL.

Treatment-related parameters and site of infec­tion in survivors and non-survivors are shown in [Table 4] and [Table 5]. The highest incidence was that of infection originating from the genital tract (n = 47, 34.5%). This is because of the higher number of female patients in the study who presented with post-partum, post-abortion or post-gynecological intervention sepsis and AKI. A significant proportion of patients (15.4%) presented with sepsis, with the source of infection being unidentified. Mortality in this group (57.1%) was higher as compared with the overall mortality. Mortality was high (64.2%) in the group of patients with respira­tory tract infection. A high proportion of mor­tality (66.6%) was also seen in patients with endovascular infection, which was due to the indwelling central catheters. Mortality was higher than average in the group of patients with skin and soft tissue infection as well (57.1%).
Table 4: Treatment-related parameters in survivors and non-survivors.

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Table 5: Site of infection in survivors and non-survivors.

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The mean SOFA score [Table 5] was 8.68. The SOFA score was significantly lower in survivors (6.79) as compared with non-sur­vivors (11.43) (<0.001). About 54.7% of the non-survivors had a SOFA score of >11. Among patients with SOFA score >11, the mortality was 85.3%. The overall outcome included complete recovery in 51.47%, partial recovery in 7.35% and ESRD in 2.2% of the patients; 38.97% of the patients died.

Patients under the age of 50 years had a higher proportion of complete recovery as compared with those above 50 years (60.6% vs 22.6%, [Table 6]). In contrast, the proportion of patients who had partial recovery or developed ESRD was higher in those above 50 years (25.8%) compared with those below 50 years of age (4.8%). The outcome was similar in both males and females, with ~51% of both showing complete recovery and ~9% of fe­males and ~10% of males having partial reco­very or developing ESRD.
Table 6: Outcome based on age-group among the study patients.

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Correlation of duration between onset and presentation, with urine output with serum creatinine

There was a positive correlation between duration of onset and presentation and SCr at the end of follow-up, with the Pearson's correlation coefficient being 0.23 and the P-value being 0.03. The correlation between urine out­put and SCr at the end of follow-up showed a negative correlation, with Pearson's correla­tion coefficient being 0.18 and P-value being 0.08. Although a significant correlation was not observed, a trend toward negative corre­lation between urine output and SCr levels was observed. An increase in the number of organs involved was associated with increasing morta­lity. The mortality was 6.66%, 12.5%, 41.6%, 83.8% and 90.9% with involvement of one, two, three, four and five organs, respectively.

   Discussion Top

A total of 136 patients were included in the analysis of the present study. Although the total number of patients appears to be on the lower side, it may be because, in the present study, all the patients who had or who could not be excluded from having chronic renal impairment, like patients with diabetes mellitus, hypertension and others, were excluded.

The maximum number of patients was in the 12-30 years age-group. This was true even when both survivors and non-survivors were considered separately. This is in contrast with other studies, where the mean age was more than 50 years. [8],[11],[12] All the other studies were conducted on the Western population, whereas the present study was performed in a deve­loping country where a higher incidence of most diseases is found in the younger age-group. The PROGRESS registry for sepsis re­vealed that the mean age for patients from India was lower as compared with that of de­veloped countries. [13] However, it should be noted that the proportion of patients greater than 50 years of age was higher in non-sur­vivors as compared with survivors. This is in accordance with various studies that show a higher mortality with increasing age. [14],[15]

The present study shows a higher proportion of females overall and also in the survivors and non-survivors groups. This might be be­cause of the fact that the present study, which was conducted in a developing country, had a higher incidence of patients with post-partum sepsis. The incidence of post-partum complica­tions, being lower in developed countries, generally show a higher proportion of males. [11],[12],[16],[17]

It was found that the time period was signifi­cantly longer among non-survivors as com­pared with survivors. The longer the elapsed period from the initial injury to the initiation of proper treatment, more is the severity of the illness, which might contribute to the higher mortality. Previous studies are also supportive of this finding. [9],[18]

There was no significant difference in the tem­perature and heart rate between the survivors and non-survivors. This is comparable to one other study, where the mean temperature and heart rate were 37°C and 95/min, respectively and a higher heart rate was found to be asso­ciated with a higher mortality. [15]

Both systolic and diastolic blood pressures were significantly lower in the non-survivors as compared with the survivors. This is in accordance with another study, [17] which found significantly lower systolic and diastolic blood pressures in the non-survivors. Two other studies also [19],[20] showed that hypotension was associated with higher mortality in critically ill patients with AKI.

Patients in both groups had a high respiratory rate, and there was no significant difference between survivors and non-survivors. A higher respiratory rate was found in patients with septic AKI as compared with other patients who had non-septic AKI or no AKI. [11]

It was found that oliguria or anuria was more commonly seen in non-survivors (88.6%) as compared with survivors (74.7%). This is in accordance with reports from two other studies, [9],[19] which found that oliguria was asso­ciated with increased mortality.

It was found that the hemoglobin levels were significantly lower (8.0 g/dL) in non-survivors as compared with survivors (9.3 g/dL). Although the difference was significant, its clinical im­plication is difficult to interpret as both the groups had low hemoglobin levels. In a pre­vious study, [12] patients with AKI due to sepsis had lower hemoglobin. In the PICARD study also, lower hemoglobin was found in patients with AKI.

The difference in the counts was not signi­ficantly different between survivors and non-survivors. An earlier study found that the leu­kocyte count was significantly higher in pa­tients with septic AKI as compared with those with sepsis and no AKI and non-septic AKI. The PICARD study [8] also showed a higher leukocyte count in patients with critical illness and AKI. However, another study [12] did not find any difference between patients with sepsis who did or did not have AKI.

Significant difference was observed in the PT and aPTT between the survivors and non-survivors, with the latter having a higher value. This indicates a higher prevalence of coagulation abnormalities in these patients. However, in an earlier study, [12] it was found that patients with sepsis and AKI had lower PT and higher aPTT as compared with those without AKI.

It was found that values of both urea and creatinine were significantly lower in the non-survivors as compared with the survivors. In an earlier study, [15] a higher blood urea and a lo­wer SCr was associated with higher mortality. In another study, [17] a higher blood urea and higher SCr was noted in survivors as com­pared with non-survivors. Additionally, one study [21] showed that a higher SCr at first dia­lysis was associated with higher mortality, while another study [13] showed that a higher blood urea is associated with higher mortality. Thus, there is no clear data regarding the predictive value of blood urea and SCr. An explanation for lower values in non-survivors might be because those who developed renal involvement later had a higher mortality. Attempts have been made to explain the va­riation that higher blood urea may be asso­ciated with increased protein catabolism, a subtle sign of metabolic stress. Low serum creatinine, particularly after adjustment for age and gender, probably reflects loss of muscle mass; however, it could also be related to vo­lume overload or inflammation, whereas blood urea may be affected by additional factors (e.g., gastro-intestinal bleeding, nutritional sup­plementation and corticosteroid use), poten­tially overcompensating for the volume-related effect. In the present study, the absence of overcompensating factors in most of the patients might explain the lower blood urea in the non-survivors.

There was no significant difference between the survivors and non-survivors with respect to the serum electrolytes (sodium and potassium). In one study, [22] the mean serum sodium and potassium levels were found to be normal and no significant difference was observed between septic and non-septic patients.

Although the mean values of bilirubin and SGPT were higher in the non-survivors as com­pared with the survivors, it was not statistically significant. In one study, [22] patients with septic AKI were found to have higher bilirubin levels compared with the other sub-groups. In another study, [15] higher serum bilirubin and in yet ano­ther study, [17] higher SGPT levels were observed in non-survivors compared with survivors.

D-dimer is a product of fibrinolysis, which is considered to have a prognostic value in pa­tients with sepsis, and was found to have an elevated mean value of 1828 ng/mL in our study patients. Non-survivors were found to have significantly higher values as compared with survivors. Even when analyzed as the proportion of survivors and non-survivors having elevated values (>500 ng/mL), the dif­ference persisted. This shows that an elevated D-dimer level is associated with higher mortality. In another study, [23] it was shown that increasing D-dimer levels predicted both multi­system organ failure and mortality.

One of the newer markers for sepsis, PCT was found to be elevated in all the patients. The mean value was 42.69 ng/mL. A trend for higher PCT values was seen in non-survivors compared with survivors. Although the usual cut-off value for indication of sepsis is 0.25 ng/mL, a higher cut-off of 2 ng/mL indicates more severe sepsis. Using this cut-off, it was seen that all the non-survivors had a high value. However, 85% of the survivors also had a value above 2 ng/mL, although this diffe­rence was not statistically significant.

There is high mortality associated with the requirement of vasopressor and ventilator sup­port. In one study, [9] it was shown that the mortality was 79.4% in the presence of shock (systolic blood pressure <90 mmHg) and 81.8% in those requiring mechanical ventilation. Simi­larly, other studies [18],[19],[20] have all shown that hypotension and mechanical ventilation are associated with higher mortality.

The survivors underwent almost double the number of HD sessions as compared with the non-survivors (11.9 vs 6.0). This discrepancy may be because of the earlier mortality in the non-survivors group. All the patients in the present study underwent HD. This might be because the study was performed in a tertiary institute and only patients with established renal failure were referred here. Another rea­son might be that only those with renal failure were considered for admission compared with those with less-severe involvement. In one report, [24] dialysis was required in 82.4% of the patients of septic AKI.

The duration of hospital stay of survivors was almost thrice as that of non-survivors (27.9 vs 8.3 days), the difference being statistically sig­nificant. This may be because of the fact that the patients who expired did so during the early part of their hospital stay. A similar pat­tern has been seen with other studies. One study [17] reported that the length of hospital stay for non-survivors was 9.3 days compared with 16 days in survivors. Data from the PROGRESS registry [13] also shows that non-survivors had a shorter hospital stay as com­pared with survivors in all the countries studied. Indian data from the same registry shows the average stay for non-survivors to be 11.9 days, whereas it was 16.2 days for the survivors.

Infection could be localized to a particular source in ~85% of the patients. In ~15% of the patients, the source remained unknown. In comparison with other studies, [11],[16],[22],[25] it can be seen that the major site of infection in other studies was the respiratory tract. However, in the present study, the major source of infection was urogenital, seen in 34.5% of the cases. This is because of the fact that females cons­tituted the majority of the patient population and had sepsis following delivery, abortion or gynecological interventions. In one study, [11] the source of sepsis remained unknown in 23.4% of the patients. Analysis of mortality associa­ted with different sources of infection showed that although the genital source of infection was the most common, almost three-fourths of the patients survived (74.4%), and mortality was seen in only one-fourth of the patients, which was lower than the overall mortality. Among patients with unknown source of in­fection, mortality (57.1%) was higher as com­pared with the overall mortality. A high pro­portion of mortality was also seen in patients with endovascular infection (66.6%), respira­tory infection (64.2%) and skin and soft tissue infection (57.1%).

The severity scoring for critically ill patients, the SOFA score, was evaluated in the patients. The mean score was found to be 8.68, and was significantly higher in non-survivors as com­pared with survivors. Among patients who had a SOFA score of >11, the mortality was high at 85.3%. Thus, SOFA score correlated well with mortality, with a higher score being associated with higher mortality. This is in accor­dance with various other studies that have shown similar results. [11] Another study, [17] showed that the APACHE score was significantly higher in non-survivors compared with survi­vors (28 vs 19). It has also been reported that patients with AKI had a higher SOFA score as compared with those without AKI. [25]

The major outcomes were either complete recovery or death, with a minority developing altered renal function or developing ESRD requiring dialysis [Table 6]. In a study, [18] where outcomes were studied in critically ill patients with AKI, the overall mortality was found to be 60.3% and dialysis dependence on discharge was 13.8% among the survivors. In another study, [26] where the recovery pattern in patients with acute tubular necrosis (ATN) re­quiring renal replacement therapy was studied, the overall mortality was 47%. Of the survi­ving patients, 57% had normal renal function, 33% had mild to moderate renal failure and 10% had severe renal failure. It has been re­ported that the frequency of occurrence of ESRD in patients with biopsy-proven ATN was 6.4% at the end of one year and 11.2% at the end of five years. [27]

A positive correlation between time to pre­sent to the hospital from initial insult and a negative correlation between urine output on admission and creatinine were seen. An earlier study [28] found that preserved urine output cor­related positively with renal recovery. It has also been reported that the severity of illness was an important predictor of renal recovery. [15] However, various other studies [29],[30] have found that none of these factors or only pre-existing renal disease were predictive of development of irreversible renal failure.

It was seen that increasing severity of illness, as observed by increasing the number of organs involved, was associated with increasing mor­tality. The least mortality of 6.6% with just one organ involvement contrasted largely from the mortality of >90% when five organs were involved. This has been observed by various other studies, [9],[18],[21] all of which have shown that increase in number of organs involved or increasing severity scores is predictive of higher mortality.

Our study suggests that the most common renal manifestation of sepsis is AKI, which is a risk factor for mortality in sepsis syndrome. Delayed presentation, requirement of ventilator/vasopressor, hypotension, low Hb, createnine, blood urea, platelets, anuria and higher PT, APTT, D-dimer, PCT and SOFA score are all indicative of the severity of illness, and were found to be significantly higher in non-survivors. SOFA score >11 and multi-organ dysfunction are risk factors for mortality.

Disclosure: Conflict of interest, financial support: None

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Correspondence Address:
Pankaj R Shah
Department of Nephrology and Clinical Transplantation, IKDRC-ITS, Civil Hospital Campus, Asarwa, Ahmedabad 380016, Gujarat
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/1319-2442.111089

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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]

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