Clinical surveillance of split renal function in en bloc kidney transplant recipients using ^99mTc-diethylenetriamine-pentaacetic acid (DTPA) dynamic renal scintigraphy: preliminary findings and novel insights

Introduction

En bloc kidney transplantation (EBKT) from infant and neonatal donors involves transplantation of a pair of kidneys from the donor into a recipient and was first reported in 1969 (1). Following transplantation, the en bloc grafts have been shown to grow rapidly in organ transplant recipients (2,3). Recent articles have shown that EBKT is associated with excellent long-term allograft performance and patient survival (4-7). It is worth noting that while EBKT involves the simultaneous transfer of both kidneys, the outcomes for each graft do not have to be aligned.

Proper assessment of graft status is critical when studying EBKT (8). Reliable assessment of split renal function after EBKT is paramount because of developmental differences between the two transplanted kidneys and the high risk of unilateral vascular complications (9-11). Dynamic renal scintigraphy can be applied in selected EBKT patients to provide clinicians with important additional information to make diagnostic decisions (8,12,13). Dynamic renal scintigraphy with ^99mTc-diethylenetriamine-pentaacetic acid (DTPA) can be used to quantify real changes in renal function and investigate potential causes of function impairment (8). ^99mTc-DTPA is filtered by glomeruli and not reabsorbed by the renal tubules. It can be used as a simple, fast, and inexpensive way to calculate glomerular filtration rate (GFR). During the examination, there is no requirement for blood or urine samples, and dietary habits do not influence the results. GFR refers to the volume of ultrafiltrate generated by the kidneys over a specific period and is regarded as the most comprehensive indicator of kidney function (14). Postoperative assessment of graft function is commonly conducted through the measurement of serum creatinine (Scr) concentration or the calculation of estimated glomerular filtration rate (eGFR). These methods are favored due to their simplicity and cost-effectiveness in clinical practice. Nevertheless, it is important to recognize that serum creatinine serves as a delayed indicator of renal impairment, meaning it may not reveal issues until significant damage has occurred. This limitation is particularly relevant in instances of renal dysfunction, as the presence of one healthy kidney may obscure mild dysfunction in the other. Consequently, relying solely on Scr as a marker may lead to undetected renal issues, highlighting the need for more sensitive monitoring techniques to ensure early identification of any potential renal deterioration (15). One advantage of using dynamic renal scintigraphy to assess renal function rather than a serum marker is that it enables individual evaluation of the function of each transplanted kidney (8). The details of surgical technique part have been described and published (16). Studies of differences in the development of EBKT kidneys are sparse. Therefore, this study aimed to examine kidney developmental differences and evaluate split renal function in EBKT recipients using ^99mTc-DTPA dynamic renal scintigraphy and other methods. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-861/rc).

Methods

Patients

This retrospective analysis examined the imaging data from 14 EBKT recipients who had undergone a procedure known as ^99mTc-DTPA dynamic renal scintigraphy from the Union Hospital of Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China, from April 2017 to November 2019. Due to the nature of this study, sample size was based on available patients and not statistical considerations. The inclusion criteria were as follows: (I) dynamic renal scintigraphy was performed on EBKT patients at our institution; (II) conducting standardized dynamic renal scintigraphy with satisfactory image quality. The exclusion criteria were as follows: (I) age of the donors was older than 1 year; (II) the imaging agent utilized for dynamic renal scintigraphy was not ^99mTc-DTPA; (III) previously undergone a kidney transplant prior to EBKT (Figure 1). All recipients exhibited negative results for both panel reactive antibodies and lymphocyte cross-matching. Donor kidneys were harvested from brain-dead or non-heart beating infants. The donors’ weight and date of birth were recorded. The induction regimen of the recipients was rabbit anti-human thymocyte immunoglobulin and methylprednisolone. The maintenance immunosuppressive agents consisted of a triple-drug regimen included tacrolimus, mycophenolate mofetil, and prednisolone. All biochemical tests were obtained from the Union Hospital of Tongji Medical College, Huazhong University of Science and Technology. Donor age and weight and pretransplant characteristics of recipients were recorded. Clinical data were collected from the medical records at the time of ^99mTc-DTPA dynamic renal scintigraphy, including age, gender, body weight, height, liver and renal function indicators, and renal ultrasound data. Kidney function indicators included Scr, blood urea nitrogen (BUN), cystatin-C. All biochemical tests were obtained within 24 hours of ^99mTc-DTPA dynamic renal scintigraphy; ultrasonography was performed within a week of ^99mTc-DTPA dynamic renal scintigraphy. The normal range for Scr, as assessed through the enzymatic method, varies based on gender. For men, the normal range is established between 0.6 and 1.2 mg/dL, whereas for women, the range is slightly lower, falling between 0.5 and 1.0 mg/dL (17).

Figure 1 Patient selection flowchart. EBKT, en bloc kidney transplantation; DTPA, diethylenetriamine-pentaacetic acid.

To enhance clarity in both the presentation and discussion of the findings, the EBKT kidneys are designated as lateral and medial. This labeling is based on their relative positions within the pelvis, rather than identifying them simply as right and left. Patients were also grouped according to timing of imaging after EBKT: the early group underwent imaging within 12 months of EBKT while the late group was imaged later. Twelve months was used as the cutoff for two reasons. First, kidneys from donors weighing ≤5 kg show progressive and significant improvement in function over the first year after EBKT (4,18). Second, eGFR and allograft survival rates do not significantly differ between grafts from pediatric EBKT donors and single-kidney grafts from adults 1 year after transplantation (18,19).

Ethics approval

This study was a retrospective observational study of EBKT patients. Individual consent for this retrospective analysis was waived. The study was performed in accordance with the Declaration of Helsinki (as revised in 2013) and approved by the ethics committee of Union Hospital, Tongji Medical College, Huazhong University of Science and Technology (No. 20210646). In addition, each organ transplantation was evaluated and authorized by the hospital’s ethics committee.

^99mTc-DTPA dynamic renal scintigraphy (Gates’ method)

Gates’ glomerular filtration rate (gGFR) was assessed by ^99mTc-DTPA dynamic renal scintigraphy. Prior to the examination, patients received adequate hydration, with an intake of 300 to 500 mL of water approximately 20 minutes before the procedure began. The scintigraphy itself was conducted utilizing an advanced integrated single-photon emission computed tomography (SPECT) and computed tomography (CT) system, which was specifically designed with low-energy high-resolution collimators to enhance imaging clarity and accuracy (Symbia T6; Siemens, Munich, Germany and Discovery 640; GE Healthcare, Chicago, IL, USA). The transplanted kidney in the iliac fossa was situated beneath the scanning probe, which was positioned ventrally, and the distance between the skin and the detector was adjusted to 5 cm (matrix size, 64×64; energy peak, 140 KeV; energy window, 20%). Prior to the injection of the radiotracer, CT imaging was conducted using the same SPECT/CT system while the subject was breathing freely. To minimize artifacts, both upper limbs were positioned on the chest, outside the area covered by the scan. Imaging procedures were conducted at a specific location, including the renal hilum, utilizing a rapid localization mode to optimize the capture of anatomical details. Subsequently, patients received an injection of 5 mCi (185 MBq) of ^99mTc-DTPA, administered as a rapid bolus. The anterior images were systematically acquired at two-second intervals for the initial 60 seconds, followed by one frame being captured every minute for an extended period ranging from 10 to 20 minutes. Specifically, the radiopharmaceutical injection should be followed by opening the imaging program and taking images as soon as possible. In the first 60 seconds of collection, the image displays information about blood perfusion at the examination site. Next, one frame was taken every 60 seconds during the functional phase of the transplanted kidney parenchyma. The radioactive counting rate of the syringe was assessed by employing the central probe both prior to and following the injection. To establish the total amount of the injected dose, the post-injection count was subtracted from the pre-injection count, with each measurement taken over a duration of one minute. Subsequently, all gathered data underwent analysis at the post-processing workstation, utilizing a pattern specifically designed for transplant kidney evaluations (Xeleris, GE Healthcare). These were operated by three highly experienced nuclear medicine physicians. The region of interest was delineated manually on the kidney’s outline, with a semi-lunar background positioned at the outer margin of the renal structure (Figure 2). The depth of the kidney was assessed using low-dose CT scans. An evaluator chose a central slice of the CT for each kidney, visually locating the most anterior and posterior points of the kidney on the image and measured the perpendicular distance from the ventral skin to these two identified points (Figure 3). The renal depth was established by averaging the two measured distances. Once this value was determined, it was input into an online system specifically designed for this purpose. Following the entry of the patient’s renal depth, gGFR was automatically computed using software that is commercially available. The graft depth inaccuracy problem associated with conventional ^99mTc-DTPA dynamic renal scintigraphy has been addressed by the anterior image acquisition and CT-assisted measurement of kidney depth (20,21). According to Gate’s modified method (22,23), GFR is calculated as follows in Eqs. [1,2]:

Total renal uptake percent=(R−RB)/e−μχR+(L−LB)/e−μχLPre−Post×100%[1]

GFR=Total renal uptake percent(%)×9.81270−6.82519[2]

Figure 2 A schematic diagram of EBKT recipients who underwent ^99mTc-DTPA dynamic renal scintigraphy. A simplified schematic of the recipient after EBKT is shown. ^99mTc-DTPA dynamic renal scintigraphy shows two kidneys transplanted into the right pelvis with normal perfusion (radiopharmaceutical is evident in the transplants within 3 to 4 seconds of iliac vessel visualization). Excretion images demonstrate normal excretion from both kidneys with expected accumulation of radiotracer in the bladder. Region-of-interest analysis of renal grafts (red circle) and background (yellow circle) activity, which allows for calculation of relative functioning renal mass. EBKT, en bloc kidney transplantation; DTPA, diethylenetriamine-pentaacetic acid.

Figure 3 Axial computed tomography imaging. Transplanted kidneys are labeled lateral and medial according to their relative position in the pelvis. (A) Measurements for the lateral kidney. (B) Measurements for the medial kidney. In the cross-sectional slice through the hilum of each kidney, the maximum and minimum kidney depths were measured, and the arithmetic mean was calculated. a, the minimum depths of the lateral kidney; b, the maximum depths of the lateral kidney; c, the minimum depths of the medial kidney; d, the maximum depths of the medial kidney.

R, right kidney counts, RB, right kidney background counts, L, left kidney counts, LB, left kidney background counts, Pre, pre-count, Post, post-count, χR, right kidney depth, χL, left kidney depth

eGFR calculation

eGFR was calculated using the Asian modified Chronic Kidney Disease Epidemiology Collaboration (CKD-EPI) equation, which changes based on patient gender and Scr (24).

Ultrasonography

Color Doppler ultrasonography can be used to demonstrate blood flow and its direction (25). Ultrasonographic examinations were performed by expert operators using Philip EPIQ7 Ultrasonography (Philips Medical Systems, Andover, MA, USA) with sector array transducer for kidney’s examination. Patients were in the supine or near-to-supine position. Following criteria were considered adequate for an ultrasonographic examination: (I) a clear longitudinal scan showing the renal parenchyma, (II) the intrarenal vascular blood flow can be visualized in a good color Doppler image, and (III) Each renal area should have at least three consecutive Doppler time-velocity spectra (upper, middle, and lower regions). Waveforms and renal Doppler resistive index (RI) were recorded. The RI is a measure of the resistance offered by the vessel to blood flow (26). Each kidney area was measured three times, and the average values were calculated to yield an index for the entire organ. Renal Doppler RI values exceeding 0.70 were deemed abnormal, while normal values fell within the range of 0.55 to 0.70. Morphological changes, including size, corticomedullary differentiation, and parenchymal echogenicity of the transplanted kidney, may occur in grafts with dysfunction. The early peak systolic and end-diastolic flow velocities were measured.

Statistical analysis

Normality of continuous data was inspected graphically and examined using the Shapiro-Wilk test. Continuous data with a normal distribution were presented as means with standard deviation and were compared using the t-test; skewed data were presented as medians with interquartile range (IQR). Correlation between variables was examined using Pearson’s or Spearman’s correlation analysis as appropriate. A two-sided P value <0.05 was considered significant. Reliability analysis was conducted using intraclass correlation coefficient (ICC). The ICC varies between 0 and 1. Generally, a value between 0 and 0.2 reflects poor consistency, while a range of 0.21 to 0.4 signifies fair consistency. Values from 0.41 to 0.6 represent moderate consistency, those from 0.61 to 0.8 indicate strong consistency, and scores between 0.81 and 1.0 demonstrate very strong consistency (27). All confidence intervals (CIs) reported are 95% CIs. Statistical analyses were conducted utilizing SPSS software version 23.0 (IBM Corp., Armonk, NY, USA).

Results

Patient characteristics

Patient characteristics before EBKT and at the time of ^99mTc-DTPA dynamic renal scintigraphy, including the time from EBKT to scintigraphy, are shown in Table 1. Among the 14 patients, nine were women and five were men. Mean age was 28.9 years (range, 15–48 years). Mean body mass index was 18.5±2.1 kg/m². Median donor age was 27.5 days (range, 6–132 days). The median recipient-donor weight ratio was 13.40 (range, 7.92–38.46). After transplantation, all patients reported complete abstinence from smoking and alcohol.

Correlation analysis

gGFR correlated positively with number of months post-transplantation (r=0.718, P=0.004). The 95% CI is 0.453–0.922. For the eGFR based on serum creatinine (70.69±33.42 mL/min) and gGFR (53.44±19.21 mL/min), ICC was 0.861 (P <0.001).

Intrarenal hemodynamics and gGFR

Intrarenal hemodynamics and gGFR for lateral and medial kidney grafts are presented in Table 2. The arcuate renal artery RI was significantly lower in medial grafts (0.59±0.05 vs. 0.54±0.07; P=0.010); the other arterial resistance indices were similar between lateral and medial kidney grafts. All indices were within normal limits (0.55–0.70). gGFR was significantly higher in medial grafts (45.34±18.66 vs. 32.29±16.80 mL/min; P=0.004).

Comparison of early and late groups

Patient characteristics and calculated GFRs according to group are shown in Table 3. gGFR was significantly higher in the late group (53.44±19.21 vs. 101.83±23.87 mL/min; P=0.001). For the eGFR based on serum creatinine (70.69±33.42 mL/min) and gGFR (53.44±19.21 mL/min), ICC was 0.861 (P<0.001).

Postoperative complications

In all 14 patients, kidney function was reliant on the transplanted kidneys. Six patients experienced a complication: ureteral stricture in three and perirenal hematoma in two; the remaining patient developed cytomegalovirus antigenemia several months after surgery (Table 1). The impact of postoperative complications on split renal function is shown in Table 4. Mean total gGFR was significantly lower in patients who experienced a postoperative complication than in those who did not (53.18±21.15 vs. 95.98±27.55 mL/min; P=0.008).

Discussion

It is estimated that 60% of nephrons are formed in the third trimester with the formation ending at 36 weeks’ gestation in normal pregnancies. Li et al. reported that EBKT from preterm neonates <30 weeks’ gestation and weighing <1.2 kg has demonstrated acceptable short- to medium-term results (28). In fact, Zeng et al. demonstrated long-term survival of EBKT allografts in our institution (16). From retrospective observational data, gGFR correlated positively with time after transplantation and was significantly higher in patients evaluated more than 12 months after EBKT than in patients evaluated less than 12 months after EBKT. These findings suggest that EBKT kidneys from infant donors can provide adequate kidney function in adults and that function improves over time. Serial ultrasonography has shown that EBKT kidneys increase in size to near-adult size over the first year, an adaptation to meet the greater metabolic demand of an adult (8). It is noteworthy that pediatric kidneys possess the ability to adapt to metabolic demands without incurring hyperfiltration damage (29). Although GFR measurements in EBKT patients in the first year after transplantation are low, this is because the transplanted kidneys are from pediatric donors. Multiple articles have demonstrated that in the early post-transplantation period, EBKT recipients exhibit a higher incidence of graft loss and lower GFR than recipients of living-related donor kidneys; however, these differences become indistinguishable after 5 years (6,18). ^99mTc-DTPA dynamic renal scintigraphy might help to differentiate between normal graft development and complications (30). In our study, patients 3 and 5 underwent ^99mTc-DTPA dynamic renal scintigraphy 12 months after EBKT (Table 1). However, gGFR was higher in patient 3, who developed a ureteral stricture, than in patient 5, who experienced no complications. Graft function in patient 5 was gradually improving during follow-up, even though the donor age was only 6 days. Additionally, patients 11 and 14 underwent ^99mTc-DTPA dynamic renal scintigraphy 19 months after EBKT. Graft function in patient 11 was nearly twice that of patient 14, who developed a ureteral stricture, even though patient 11’s donor was only 11 days old. In some patients who developed a ureteral stricture, ^99mTc-DTPA dynamic renal scintigraphy showed good tracer uptake on the affected side with impaired tracer wash out during the excretory phase; dynamic renal scintigraphy accurately determined the level of obstruction. Therefore, clinicians should carefully check postoperative imaging to differentiate a typically developing EBKT kidney from one developing a complication that causes low GFR.

Kidney function was significantly better in EBKT patients who did not develop postoperative complications. gGFR was lower in both the medial and lateral kidneys in patients who experienced complications than in patients who did not; however, it did not differ between the two kidneys. Postoperative complications are a crucial factor which affects recovery and development of graft function in EBKT patients. Appropriate management of complications is also important for faster recovery.

Doppler ultrasonography is an effective and reliable method for following kidney transplant recipients (25,26). It can assess in vivo renal blood flow parameters and deliver rapid, reproducible imaging data; however, it is unable to provide accurate GFR values. In our study, gGFR was higher in medial kidney grafts, which was reflected in the arcuate renal artery resistance indices. In addition, gGFR was higher in medial kidneys than lateral ones in patients without complications. The discrepancy in graft development can be attributed to several factors. The renal graft artery was anastomosed to the common iliac artery (Figure 1A). Because the medial kidney was located below the lateral one, the angle between the transplanted renal artery and the iliac vessel for the medial kidney was narrow. In addition, the location of the medial graft was relatively fixed and the degree of variation relatively small. As a result, these contribute to relatively appropriate blood supply after surgery.

Scr, BUN, and cystatin-C are excellent markers of renal function in patients with impaired kidney function. Various elements, including dehydration, protein consumption from diet, muscle mass, and the use of diuretics, can affect Scr levels (31). When patients are stratified according to gGFR values, an increase in Scr will not be observed until GFR decreases substantially. Scr might not serve as the most precise and sensitive indicator of early alterations in kidney function, since renal damage may not be reflected in Scr level for many hours or even days. We also found that eGFR based on the Asian modified CKD-EPI equation was higher than the gGFR determined with ^99mTc-DTPA dynamic renal scintigraphy. Another study has shown that the CKD-EPI equation, derived from an extensive dataset compiled from both clinical and research cohorts, demonstrates greater accuracy and broader usage compared to other GFR estimation techniques in Chinese patients with chronic kidney disease (32). Nevertheless, the primary factors influencing the equation are gender, age, and serum creatinine levels, meaning alterations in these factors will impact the calculated eGFR. Furthermore, the equation was devised for clinical application in patients with native kidneys, not transplants. We found that ^99mTc-DTPA dynamic renal scintigraphy is more reliable to evaluate renal function in the first year after EBKT; eGFR calculated using the Scr-based CKD-EPI equation can be used afterwards. This should be validated in future prospective studies.

There are several limitations in this study. First, it was retrospective and had a small sample size. Some data were not able to be completely supplemented and further analyzed. Second, individual renal grafts in the iliac fossa may experience mild torsion and a small degree of overlap. Third, the impact of assessment of split renal function on long-term allograft outcome was not demonstrated. We will further increase our number of subjects and continue following these patients to provide a more comprehensive understanding and establish a gGFR cutoff for diagnosing declining graft function in EBKT patients.

Conclusions

We conclude that gGFR may reflect changes in split renal function in EBKT recipients. ^99mTc-DTPA dynamic renal scintigraphy monitoring is feasible and effective to assess renal function and complications after EBKT.

Acknowledgments

We thank Liwen Bianji (Edanz) (https://www.liwenbianji.cn) for editing the language of a draft of this manuscript. Some parts of the manuscript were first presented as a conference abstract (visit: https://link.springer.com/chapter/10.1007/978-981-19-8899-8_24). We thank the organizers of the 23rd Pacific Basin Nuclear Conference (PBNC 2022) for the opportunity to present our research verbally in the oral presentation session.

Funding: This research was supported by National Natural Science Foundation of China (No. 81771866).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-861/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-861/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. This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the ethics committee of Union Hospital, Tongji Medical College, Huazhong University of Science and Technology (No. 20210646) and 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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