The value of intrarenal resistive index in delayed graft function after kidney transplantation

Introduction

Chronic kidney disease (CKD) represents a global public health problem; the global prevalence of CKD is about 14.3%, of which about 2% of CKD patients will progress to end-stage renal disease (ESRD), and the number of patients continues to grow. When CKD progresses to ESRD, patients can only stay alive with renal replacement therapy, which mainly includes dialysis therapy and kidney transplantation. Kidney transplantation is the optimal choice for patients with ESRD. Successful kidney transplantation can improve the quality of life, reduce medical costs, and increase patient survival, and its therapeutic effect is significantly superior to that of long-term dialysis treatment (1).

Delayed graft function (DGF) is an early complication after kidney transplantation affecting the function of a transplanted kidney. It is a state of acute kidney injury, which manifests with postoperative oliguria and increased biochemical markers, such as serum creatinine (SCr) and serum urea nitrogen (SUN). DGF is associated with decreased graft survival, resulting in prolonged hospitalization and increased medical costs (2). Its underlying pathogenesis is complex, and various potential mechanisms, including the donor proinflammatory status, ischemia/reperfusion (I/R) injury, and the activation of innate and adaptive immune response might contribute to graft damage (3). At present, a consensus has not been reached on the definition of DGF; we therefore referred to the definition in the Technical Specification for the Diagnosis and Treatment on Delayed Graft Function after Renal Transplantation (2019 edition), specifically, the need for dialysis during the first week after transplantation or a daily SCr decrease of less than 10% of the previous 1 day in the first 3 postoperative days or that the patient’s SCr had not decreased to 400 µmol/L at 1 week postoperatively (4).

With the increased sensitivity of definition and the use of donation after cardiac death, the incidence of DGF has been increasing in recent years. Since there is currently no effective treatment, early prediction and timely intervention are crucial to the recipients. In recent years, ultrasound has become the main imaging method for clinical monitoring of renal transplantation due to its low cost, non-invasiveness, and ease of application. In China, clinicians recommend that patients undergo review ultrasound once a day within 7 days after kidney transplantation to assess whether there are abnormalities in the blood vessels, parenchyma, collection system, and perirenal area of the transplanted kidney. Abnormal ultrasound-related parameters may alert clinicians to the risk of DGF in patients. Therefore, ultrasound has also become the primary clinical tool for early evaluation of DGF in patients after kidney transplantation (1). Two-dimensional (2D) ultrasound can measure the length, width, and thickness of transplanted kidney, and observe the parenchymal echo and cutaneous medullary demarcation of the transplanted kidney. Doppler ultrasound (DUS) can supply spectral parameters of a transplanted kidney, including peak systolic velocity (PSV), end-diastolic velocity (EDV), and resistive index (RI).

The aim of this study was to investigate the application value of DUS, especially intrarenal RI, in the evaluation of DGF after kidney transplantation by comparing the ultrasound results between DGF patients and normal graft function (NGF) patients. Meanwhile, the demographic characteristics and clinical information in these patients were analyzed. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1530/rc).

Methods

Study design and patients

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and approved by the Biomedical Ethics Review Committee of West China Hospital of Sichuan University (No. 468 Year 2020 Audit). The requirement for individual consent for this retrospective analysis was waived. Patients who underwent kidney transplantation at West China Hospital of Sichuan University from 1 July 2019 to 1 April 2023 were collected retrospectively. According to whether their postoperative renal function returned to normal, the patients were divided into a DGF group and an NGF group. The inclusion criteria of patients in the DGF group were as follows: (I) dialysis was required during the first week after transplantation; (II) the daily SCr decrease was less than 10% of the previous 1 day in the first 3 postoperative days; or (III) the patient’s SCr had not decreased to 400 µmol/L at 1 week postoperatively (4). The exclusion criteria were as follows: (I) age <14 years, pregnancy, lactation period, severe cardiopulmonary disease; (II) non-first-time kidney transplant treatment; (III) absence of conventional DUS and clinical data after kidney transplantation; (IV) the presence of other diseases that may lead to elevated RI in patients, such as hematoma with the longest diameter ≥2 cm, urinary tract obstruction, and venous thrombosis; (V) patients who refused ultrasound examination. Subsequently, in order to construct a control group, the remaining patients with normal renal function were randomly selected according to the ratio of the DGF group:NGF group =1:1, which were included in NGF group. At the same time, in order to ensure the accuracy of the experimental results, there was no significant difference in age between the 2 groups.

Demographic data [gender, age, height, weight, body mass index (BMI), medical history, dialysis method, etc.] and clinical data (heart rate, blood pressure, clinical test results) were obtained from the Hospital Information System (HIS) System of our hospital.

Ultrasound examination

DUS of the transplanted kidney was performed by a senior ultrasound doctor or sonographer with more than 10 years of experience in West China Hospital of Sichuan University, and the results were accurate and reliable. A 5-MHz convex transducer was used in the supine position. The standard settings for abdominal examinations of the given ultrasound machine were used. The maximal length, width, and thickness of the transplanted kidney were measured by 2D ultrasound, and the volume of the transplanted kidney was calculated according to the formula (kidney volume = length × width × thickness × 0.5); the parenchymal echo and corticomedullary differentiation were also observed. Blood flow was analyzed by DUS to detect vessel abnormalities of the transplanted kidney. PSV, EDV, and RI values were measured after the ultrasound doctors or sonographer had manually located the relevant blood vessels. In the process of measuring low-speed blood flow, the ultrasound doctors or sonographer first increased the spectral gain, and then the gain was gradually reduced until the background noise of the spectrum disappeared as much as possible to reduce the influence of background noise on the accuracy of the data. Renal RI was estimated using the following formula: (PSV − EDV)/PSV (2). The 2D ultrasound and DUS images of typical DGF and NGF patients are shown in Figure 1. The time of examination was within 1 week after kidney transplantation.

Figure 1 2D ultrasound and spectral DUS images of typical DGF and NGF patients. (A) 2D ultrasound image of transplanted kidney in DGF patients; (B) spectral Doppler of main renal artery in DGF patients; (C) spectral Doppler of arcuate artery in DGF patients; (D) 2D ultrasound image of transplanted kidney in NGF patients; (E) spectral Doppler of main renal artery in NGF patients; (F) spectral Doppler of arcuate artery in NGF patients. 2D, 2-dimensional; DUS, Doppler ultrasound; DGF, delayed graft function; NGF, normal graft function.

Statistical analysis

We used the statistical software SPSS 20.0 (IBM Corp., Armonk, NY, USA) to analyze all data. Categorical variables were manifested as numbers or percentages, and chi-square analysis was performed to analyze categorical data. Continuous variables were presented as means and standard deviations (SDs). When the data were consistent with normal distribution and homogeneity of variance, t-test was used to compare the differences between the 2 groups; if not, Mann-Whitney U test was used. The predictive performance and cut-off value of RI were analyzed with receiver operating characteristic (ROC) curve analysis and the analysis of the area under the curve (AUC). A P value <0.05 was considered statistically significant.

Results

A total of 225 patients were enrolled in the present study after exclusion. These included 153 male (68.0%) patients and 72 female (32.0%) patients. The mean age (± SD) of the study population was 38.4±11.6 years (range, 14–65 years). The samples were divided into DGF group (n=115, 51.2%) and NGF group (n=110, 48.8%) according to the diagnostic criteria for DGF.

Demographic information

The demographic data of patients are summarized in Table 1, which indicated that DGF patients (22.30±3.55 kg/m²) had a significantly higher BMI than NGF patients (21.31±3.53 kg/m²); the other demographic data were not statistically significant (P>0.05).

Clinical data

The DGF group showed worse kidney function values on the first postoperative day. Compared with the NGF group, the SCr, cystatin C (Cys-C), SUN, and uric acid (UA) on the postoperative 1st day in DGF group were significantly higher, and the albumin (ALB) and estimated glomerular filtration rate (eGFR) in the DGF group were significantly lower. The differences were statistically significant (P<0.05) (Table 2).

Ultrasound parameters

There was no significant difference in the size of the graft between the DGF group and NGF group, including the maximal length, width, thickness, and volume of the transplanted kidney (P>0.05). Compared to NGF patients, DGF patients displayed more obvious parenchymal changes, including enhanced parenchymal echo and loss of corticomedullary differentiation.

Except for the PSV of the segmental artery, the PSV and EDV of the transplanted kidney in the DGF group measured by DUS were significantly lower than those in the NGF group. In addition, the RI of all transplanted renal arteries in the DGF group were higher than those in the NGF group (Table 3).

The ROC curve analysis confirmed that 0.75 was the optimal cut-off RI value, and when RI >0.75, the risk of DGF significantly increased. The sensitivity was 68.7%, and the specificity was 74.3% (Figure 2).

Figure 2 ROC curves for renal artery RI in the DGF group. ROC, receiver operating characteristic; RI, resistive index; DGF, delayed graft function.

The DGF group was divided into 2 subgroups based on the time interval between kidney transplantation and the first ultrasound examination, including the <48-hour group (n=95) and the ≥48-hour group (n=20). The comparative results illustrated that except for segmental artery RI, the rest of the renal artery RI measured ≥48 h after kidney transplantation was significantly higher than that measured <48 hours after transplantation (P<0.05) (Table 4).

Further, the DGF group and NGF group were divided into a <48-hour group and a ≥48-hour group, respectively. The RIs of DGF patients measured at different times were significantly higher than those of NGF patients, which elucidated that the RI of all renal arteries can diagnose the occurrence of DGF.

The ROC curves for RI measured at the renal artery of the transplanted kidney over 2 periods are plotted in Figures 3,4. The AUC of RI measured ≥48 hours after kidney transplantation was generally greater than that <48 hours, and the AUC of the main renal artery RI measured ≥48 hours was the largest (AUC =0.86), which had the best diagnostic efficacy for DGF (Table 5).

Figure 3 ROC curves for renal artery RI measured <48 h after kidney transplantation. ROC, receiver operating characteristic; RI, resistive index.

Figure 4 ROC curves for renal artery RI measured ≥48 h after kidney transplantation. ROC, receiver operating characteristic; RI, resistive index.

Discussion

DGF is one of the most common complications after transplantation, manifesting as a form of acute kidney injury, which seriously damages the short-term kidney function and affects long-term prognosis of the transplanted kidney (5). DUS has become a valuable imaging technique in diagnostic and therapeutic assessments of renal diseases. It obtains not only the anatomical image of the transplanted kidney, but also supplies hemodynamics information (6). In our study, we showed that some ultrasound parameters, such as RI, were strong predictors of DGF, specifically, increased RI may mean poor recovery after kidney transplantation, which has been emphasized in some previous studies (7-9). In order to ensure the accuracy of the experimental results, we paid special attention to the age factor in the design of the study, so that there was no significant age difference between the 2 groups of patients, thus excluding the influence of age as a potential confounding variable on the results. However, it is worth noting that Naesens et al. proposed that renal RI does not accurately reflect the progression of renal diseases, and they pointed out that there is no direct correlation between RI and graft function, acute inflammatory lesions, or chronic histological damage (10). This view is different from our conclusion. We believe that the reason for this difference may be due to the different choice of research participants. We hope that more relevant research in the future will be able to explore this in depth. In addition, there are many other risk factors that are considered able to predict the occurrence of DGF, such as higher BMI of the receptor, poor renal function on the first day after surgery, and the presence of proteinuria (11,12). However, it should be noted that although these factors have certain indicative effects, their specificity is low, and their reliability may be affected by many factors. Therefore, in practical application, it is necessary to consider the specific situation comprehensively.

2D ultrasound may still play an important role in DGF caused by microscopic parenchymal changes, such as injury due to acute tubular necrosis (ATN) or acute rejection (AR) (13). ATN and AR can cause lymphocyte cells to attack normal graft cells, and fluid oozes out through the damaged membrane, eventually leading to obvious renal interstitial edema. Therefore, 2D ultrasound can roughly determine whether DGF has occurred by changes in kidney volume. However, our study found that there were no significant differences in the size of the graft between the 2 groups. This may be because most of the data in our study came from patients within 48 hours after kidney transplantation, and the size of the graft has not changed significantly. This conclusion needs to be confirmed by increasing the sample size and extending the postoperative follow-up time.

DUS can evaluate the renal graft perfusion indirectly by calculation of the RI and limited visualization of vessels, which has been extensively used in renal diseases both in diagnostic, prognostic, and therapeutic assessments (14). RI is an important index to evaluate the blood perfusion resistance of transplanted kidneys, with predictive value in a variety of vascular and kidney complications. The normal intrarenal arterial blood flow is low resistance, so as to maintain a high perfusion state of the kidney (15). Our study indicated that the PSV and EDV of transplanted kidney in the DGF group were lower than those in the NGF group, and RI in the DGF group was significantly higher, the mean RI of the main renal artery in DGF patients even reached 0.80, which all illustrated that the blood perfusion resistance of the DGF patients’ transplanted kidney increased significantly. The reason may be that the transplanted kidney of DGF patients had experienced I/R injury, including renal small vessel endothelial cells and tubular epithelium having been injured by ischemia and hypoxia, releasing inflammatory factors, and the aggregation of inflammatory cells to the corresponding lesions, which led to local swelling, the decrease of blood perfusion, and the increase of vascular pressure (16). The RI of DGF patients was usually higher, which is consistent with the results of most current studies (2,3,8,17).

Although a consensus on the renal RI cut-off to predict the risk of DGF has not been reached, the most frequently used cut-off was 0.70 in clinical studies. Bellos and Bogaert et al. reported that 0.70 was the optimal RI value to predict the risk of DGF, with a sensitivity of 65.6% and specificity of 73.3% (5,8). However, the results of our study revealed that 0.75 would be the optimal cut-off RI value. In addition, some researchers have considered that when RI >0.8, it indicated renal damage and decreased renal function. In an earlier prospective study by Radermacher et al., 0.795 was used as a RI cut-off for the diagnosis of DGF, and they finally attained the highest sensitivity (56.0%) and specificity (96.0%), which confirmed the accuracy of the predefined value of 0.80 (7). We speculated that the contradiction was due to a combination of factors, such as the heterogeneity in study populations, the subjectivity of the operator when measuring RI, that varied sites of renal artery RI were measured, and different types of ultrasound machines were used (18). In the spectral analysis, we observed that the PSV of the arch artery in the DGF group and the NGF group was about 20 cm/s, whereas the EDV was about 10 cm/s. It is worth noting that in the measurement of these low-speed blood flows, the noise level (usually characterized by fluctuations below the zero line) is quite close to the EDV value, indicating that there is a certain degree of signal interference. In addition, in some cases, additional noise signals may also be recorded in the centrifugal direction. To solve this problem, our experienced ultrasound doctors or sonographer first increased the spectral gain, and then the gain was gradually reduced until the background noise of the spectrum disappeared as much as possible, so as to minimize the measurement error caused by background noise.

When is RI measured with the highest predictive value? The study results of Mwipatayi et al. represented significant positive relationship between elevated RI measurement within 24 hours after transplantation and DGF. In other words, the elevated RI measurement within 24 hours may be an effective marker for early identification of high-risk allografts, especially transplanted kidneys with DGF (19). Similarly, as observed in the study of Mocny et al., the sensitivity of the mean RI value to predict DGF occurrence was the highest on the day of the transplantation, which suggested that RI sensitivity increased in the 24-hour post-transplantation period (6). However, the result of our study was in contradiction with the findings of the above studies. In the present study, the AUC of RI measured ≥48 hours after kidney transplantation was generally greater than that of RI measured <48 hours, the AUC of main renal artery RI measured ≥48 hours after kidney transplantation was the largest, which confirmed that RI measured ≥48 hours had higher sensitivity and better diagnostic efficacy in diagnosing DGF. Rodrigo et al. also concluded that the risk of elevated RI in DGF patients on days 2 to 3 was nearly 3 times higher than that in other periods (20). We suggested that the change of renal microcirculation caused by various factors, such as immunologic and non-immunologic factors, was a gradual process, which took some time and resulted in the delay in sensitivity. In the future, we need to conduct further targeted experiments to compare and verify.

This study had some limitations. First, this was a single-center retrospective study. Multiple confounding factors may affect the consistency of the data collected at different periods, such as possible bias in the selection of the population. Second, since our data were from the early postoperative period after kidney transplantation, few DGF patients had completed kidney biopsy during our observation period. Therefore, we could not collect sufficient pathological findings of DGF patients. Third, parenchymal echo, corticomedullary differentiation, and RI measurement were subjective to some degree, and would have been affected by many factors such as the type of ultrasound machine and the distance of the kidney transplant from the body surface, which may have interfered with the accuracy of the research results. Finally, we did not collect the follow-up ultrasound results of the patients. The efficacy of different treatment methods for early DGF needs to be further studied in the future.

Conclusions

DUS plays an important role in postoperative evaluation of kidney transplants, which provides hemodynamics information, especially intrarenal RI. Increased RI as a reliable predictor early in the postoperative period may indicate the occurrence of DGF, which can increase sensitivity of clinicians to identify patients at risk of DGF (19), and main renal artery RI measured ≥48 hours after kidney transplantation had the better diagnostic efficacy for DGF. Clinicians should combine the conclusions drawn from the DUS with clinical results (21), recognize DGF early to then promptly adjust the postoperative immunosuppressive regimen and improve long-term graft survival (22).

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-1530/rc

Funding: This study was supported by the National Natural Science Foundation of China (No. 82102067); the Key Research and Development Program sponsored by Chengdu Science and Technology Bureau (No. 2022-YF05-01498-SN); and 1·3·5 Project for Disciplines of Excellence–Clinical Research Incubation Project, West China Hospital, Sichuan University (No. 2020HXFH049).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1530/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and approved by the Biomedical Ethics Review Committee of West China Hospital of Sichuan University (No. 468 Year 2020 Audit). The requirement for individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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