ABSTRACT Background Current reliance on clinical, laboratory and Doppler ultrasound (DUS) parameters for monitoring kidney transplant perfusion in the immediate post-operative period in children risks late recognition of allograft hypoperfusion and vascular complications. Near-infrared spectroscopy (NIRS) is a real-time, non-invasive technique for monitoring tissue oxygenation percutaneously. NIRS monitoring of kidney transplant perfusion has not previously been validated to the gold standard of DUS. We examined whether NIRS tissue oxygenation indices can reliably assess blood flow in established paediatric kidney transplants. Methods Paediatric kidney transplant recipients ages 1–18 years with stable allograft function were eligible. Participants underwent routine DUS assessment of kidney transplant perfusion, including resistive index (RI) and peak systolic velocity at the upper and lower poles. NIRS data [tissue oxygenation index (TOI%)] were recorded for a minimum of 2 min with NIRS sensors placed on the skin over upper and lower allograft poles. Results Twenty-nine subjects with a median age of 13.3 (range 4.8–17.8) years and a median transplant vintage of 26.5 months participated. Thirteen (45%) were female and 20 (69%) were living donor kidney recipients. NIRS monitoring was well tolerated by all, with 96–100% valid measurements. Significant negative correlations were observed between NIRS TOI% and DUS RI at both the upper and lower poles (r = −0.4 and −0.6, P = 0.04 and 0.001, respectively). Systolic blood pressure but not estimated glomerular filtration rate also correlated with NIRS TOI% (P = 0.01). Conclusions NIRS indices correlate well with DUS perfusion and haemodynamic parameters in established paediatric kidney transplant recipients. Further studies are warranted to extend NIRS use for continuous real-time monitoring of early post-transplant perfusion status. Doppler ultrasonography, kidney transplantation, near-infrared spectroscopy, paediatrics, perfusion, physiologic monitoring INTRODUCTION Kidney transplantation is the treatment of choice for end-stage kidney disease, offering improved overall health outcomes, quality of life and health economic benefits relative to dialysis [1–4]. Early transplant dysfunction can occur for multiple reasons [5, 6]. Thrombosis affects 4–18% of paediatric kidney transplants and is a significant cause of graft loss within the first year [7–10]. Children <6 years of age are particularly susceptible due to smaller vessel size and relatively lower cardiac output perfusing an adult kidney [11, 12]. Appropriate fluid and/or inotropic support is paramount in order to optimize transplant perfusion. Currently, clinical and laboratory parameters such as changes in serum creatinine and urine output are used to monitor graft perfusion, with Doppler ultrasound (DUS) performed if concerns arise. These parameters do not reflect changes in the transplanted organ’s perfusion in real time, which delays diagnosis of vascular complications. DUS is the gold standard method for assessing renal allograft blood flow [13–15]. Resistive index (RI) and peak systolic velocity (PSV) are the principal indices of organ vascular resistance related to microvascular injury and interstitial oedema and patency of larger transplant vessels [16–18]. A key limitation of DUS is that it does not allow continuous real-time monitoring of perfusion in the critical early post-transplantation period. Near-infrared spectroscopy (NIRS) is a non-invasive, continuous, real-time measure of tissue oxygenation . Established applications include monitoring brain perfusion during cardiopulmonary bypass and global tissue perfusion in septic shock . Renal NIRS was found to be an early predictor of acute kidney injury in infants with congenital heart disease undergoing surgical repair . In animal models, testicular NIRS detected organ ischaemia earlier than DUS . One previous study compared NIRS measurements in paediatric transplant recipients to plasma creatinine, urine output and urinary neutrophil gelatinase-associated lipocalin (NGAL), but not to DUS . The aim of this pilot study was to assess whether NIRS can be used to assess renal allograft perfusion in stable paediatric recipients by comparing it with the current gold standard of DUS. MATERIALS AND METHODS Patient eligibility and assessment Paediatric kidney transplant recipients <18 years of age with stable allograft function at the Department of Paediatric Nephrology at Great Ormond Street Hospital were eligible. Exclusion criteria were (i) wound complications affecting skin overlying the transplant, (ii) anticipated patient’s inability to lie still for NIRS recording and (iii) intercurrent illness impacting fluid status or allograft function. Informed consent was obtained from participants and parents/caregivers as appropriate. The study was approved by a national research ethics committee and the Health Research Authority (ref: 16/LO/1897). Participants were assessed during routine transplant clinic. Assessment included a clinical history review to identify any acute intercurrent illness, physical examination for anthropometric data and blood pressure measurement, blood sampling for standard biochemistry (including plasma creatinine), estimated glomerular filtration rate (eGFR) calculation based on the Schwartz formula and renal allograft ultrasound with Doppler blood flow measurements . Blood pressures were obtained manually with Doppler amplification as per recent guidelines . Ultrasound imaging with colour flow Doppler Ultrasound transplant imaging was undertaken as part of routine annual or biannual surveillance by a single trained paediatric radiographer. The GE Logiq E9 ultrasound system with a curvilinear 1–5 MHz or linear array 5–9 MHz transducer was used for optimal signal penetration and resolution. Initial machine settings were according to the manufacturer’s recommendations (renal transplant preset) and adjustments were applied by the operator to the depth (magnification), focus, gain, dynamic range and Doppler scale (velocity range/colour gain). This was individual to each patient. The positions of transplant upper and lower poles were marked on the patient’s skin with a hypoallergenic marker. Images were reviewed by a paediatric radiologist. Measurements included peak systolic and diastolic velocities and resistive indices from both the main renal transplant artery and vein and from intrarenal vessels at the upper and lower poles. Upper and lower pole depths from the skin surface were recorded. Assessment of global and regional perfusion was made. NIRS measurements NIRS monitoring was undertaken using the NIRO 200-NX (Hamamatsu Photonics KK, Hamamatsu City, Japan). Relevant skin areas were cleaned with a chlorohexidine wipe and paediatric optodes were positioned over the upper and lower pole skin markings. External light penetration was minimized by securing an opaque adhesive membrane to the skin. NIRS measurements were recorded and displayed continuously from each pole from two separate channels for a minimum of 2 min with patients lying supine. Individual NIRS data were extracted from the NIRO 200-NX with an encrypted portable external memory disk and converted into an Excel (Microsoft, Redmond, WA, USA) document for statistical analysis. Outcome measures and data analysis The RI derived from DUS was the primary outcome and the tissue oxygenation index (TOI%) was the main explanatory variable. The mean TOI% at each pole was used for analyses, as acute changes in allograft perfusion were not anticipated. The relationship between TOI% (upper and lower pole) and RI (upper and lower pole, respectively) was evaluated using linear regression. As the distance of the tissue of interest from the infrared light source might affect NIRS measurements, the interaction between pole depth and TOI% was also examined. To further clarify the physiological significance of TOI%, its correlation with systolic blood pressure and eGFR was evaluated, as these parameters were previously reported to be associated with NIRS [23, 26, 27]. Continuous variables are expressed as mean ±standard deviation (SD) if normally distributed, otherwise as median (range). Analyses were performed using SPSS Statistics for Windows, version 21.0 (IBM, Armonk, NY, USA). ETHICAL APPROVAL All procedures performed were in accordance with the 1964 Helsinki Declaration ethical standards and its later amendments. The study was approved by a national research ethics committee and the Health Research Authority (ref: 16/LO/1897) RESULTS Patients’ characteristics Twenty-nine patients with a median age of 13.3 (range 4.8–17.8) years participated. Patients’ demographic characteristics, underlying diagnoses, transplant operation details and allograft function at the time of the study are summarized in Table 1. Table 1 Subject characteristics Age (years), median (range) 13.3 (4.8–17.8) Female, n (%) 13 (44.8) Time post-transplant (months), median (range) 26.5 (1–48.7) Diagnoses, n (%) CAKUT 15 (51.7) Ciliopathies 4 (13.8) Cystic kidney disease 3 (10.3) Inborn errors of metabolism 3 (10.3) Congenital nephrotic syndrome 2 (6.9) Other 2 (6.9) Type of transplant, n (%) Living donor 20 (69) Extraperitoneal surgical approach 19 (65.5) Systolic BP (mmHg), mean ± SD 102.9 ± 11.5 [median 102 (IQR 98–112)] eGFR (mL/min/1.73 m2), mean ± SD 52.5 ± 19.9 Age (years), median (range) 13.3 (4.8–17.8) Female, n (%) 13 (44.8) Time post-transplant (months), median (range) 26.5 (1–48.7) Diagnoses, n (%) CAKUT 15 (51.7) Ciliopathies 4 (13.8) Cystic kidney disease 3 (10.3) Inborn errors of metabolism 3 (10.3) Congenital nephrotic syndrome 2 (6.9) Other 2 (6.9) Type of transplant, n (%) Living donor 20 (69) Extraperitoneal surgical approach 19 (65.5) Systolic BP (mmHg), mean ± SD 102.9 ± 11.5 [median 102 (IQR 98–112)] eGFR (mL/min/1.73 m2), mean ± SD 52.5 ± 19.9 BP, blood pressure; CAKUT, congenital anomalies of kidneys and urinary tract; IQR, interquartile range. Table 1 Subject characteristics Age (years), median (range) 13.3 (4.8–17.8) Female, n (%) 13 (44.8) Time post-transplant (months), median (range) 26.5 (1–48.7) Diagnoses, n (%) CAKUT 15 (51.7) Ciliopathies 4 (13.8) Cystic kidney disease 3 (10.3) Inborn errors of metabolism 3 (10.3) Congenital nephrotic syndrome 2 (6.9) Other 2 (6.9) Type of transplant, n (%) Living donor 20 (69) Extraperitoneal surgical approach 19 (65.5) Systolic BP (mmHg), mean ± SD 102.9 ± 11.5 [median 102 (IQR 98–112)] eGFR (mL/min/1.73 m2), mean ± SD 52.5 ± 19.9 Age (years), median (range) 13.3 (4.8–17.8) Female, n (%) 13 (44.8) Time post-transplant (months), median (range) 26.5 (1–48.7) Diagnoses, n (%) CAKUT 15 (51.7) Ciliopathies 4 (13.8) Cystic kidney disease 3 (10.3) Inborn errors of metabolism 3 (10.3) Congenital nephrotic syndrome 2 (6.9) Other 2 (6.9) Type of transplant, n (%) Living donor 20 (69) Extraperitoneal surgical approach 19 (65.5) Systolic BP (mmHg), mean ± SD 102.9 ± 11.5 [median 102 (IQR 98–112)] eGFR (mL/min/1.73 m2), mean ± SD 52.5 ± 19.9 BP, blood pressure; CAKUT, congenital anomalies of kidneys and urinary tract; IQR, interquartile range. DUS measurements Twenty-nine kidney transplant ultrasound studies with colour flow Doppler for perfusion assessment were undertaken. No patients demonstrated significant urinary tract obstruction, perinephric collection or other acute surgical complications. All had patent transplant renal vessels without evidence of stenosis based on colour Doppler waveforms. Global allograft perfusion was normal in all recipients. PSVs, RIs and distances from the skin surface for the upper and lower graft poles are shown in Table 2. Table 2 DUS and NIRS summary data PSV (cm/s) RI Depth (cm) TOI % Upper pole 27.6 ± 7.8 0.65 ± 0.07 2.6 ± 1.2 78.8 ± 7.0 Lower pole 25.3 ± 8.0 0.65 ± 0.07 2.0 ± 0.9 79.3 ± 10.7 P-value NS NS 0.001 NS PSV (cm/s) RI Depth (cm) TOI % Upper pole 27.6 ± 7.8 0.65 ± 0.07 2.6 ± 1.2 78.8 ± 7.0 Lower pole 25.3 ± 8.0 0.65 ± 0.07 2.0 ± 0.9 79.3 ± 10.7 P-value NS NS 0.001 NS Values are expressed as mean ± SD. Table 2 DUS and NIRS summary data PSV (cm/s) RI Depth (cm) TOI % Upper pole 27.6 ± 7.8 0.65 ± 0.07 2.6 ± 1.2 78.8 ± 7.0 Lower pole 25.3 ± 8.0 0.65 ± 0.07 2.0 ± 0.9 79.3 ± 10.7 P-value NS NS 0.001 NS PSV (cm/s) RI Depth (cm) TOI % Upper pole 27.6 ± 7.8 0.65 ± 0.07 2.6 ± 1.2 78.8 ± 7.0 Lower pole 25.3 ± 8.0 0.65 ± 0.07 2.0 ± 0.9 79.3 ± 10.7 P-value NS NS 0.001 NS Values are expressed as mean ± SD. NIRS measurements A median of 838 NIRS readings per patient (range 384–2860) were obtained. NIRS monitoring was well tolerated by all participants, with a 96–100% rate of valid measurements. Summary statistics for TOI% values (upper and lower pole) are provided in Table 2. TOI% as a predictor of DUS-derived RI The TOI% in the lower and upper poles was significantly associated with the respective RIs (r = −0.60, P = 0.001; and r = −0.40, P = 0.04) (Figures 1 and 2). FIGURE 1 View largeDownload slide Correlation between NIRS TOI% and DUS RI at the lower pole (r = −0.60, P = 0.001). FIGURE 1 View largeDownload slide Correlation between NIRS TOI% and DUS RI at the lower pole (r = −0.60, P = 0.001). FIGURE 2 View largeDownload slide Correlation between NIRS TOI% and DUS RI at the upper pole (r = −0.40, P = 0.04). FIGURE 2 View largeDownload slide Correlation between NIRS TOI% and DUS RI at the upper pole (r = −0.40, P = 0.04). Univariate linear regression yielded the following prediction equations for the lower and upper pole RIs: RI lower pole = 0.941 + [−0.004 × (TOI% lower pole)] RI upper pole = 0.972 + [−0.004 × (TOI% upper pole)] There was no interaction between (lower or upper) pole depth and (lower or upper) TOI% (P = 0.24 and P = 0.29, respectively). TOI% and association with other parameters Both the upper pole and lower pole TOI% were significantly associated with systolic blood pressure but not with eGFR (Table 3). Table 3 Correlation of TOI% with systolic BP and eGFR TOI%, upper pole TOI%, lower pole Other variables r P-value r P-value eGFR −0.24 0.22 −0.30 0.11 Systolic BP 0.50 <0.01 0.45 0.01 TOI%, upper pole TOI%, lower pole Other variables r P-value r P-value eGFR −0.24 0.22 −0.30 0.11 Systolic BP 0.50 <0.01 0.45 0.01 BP, blood pressure. Table 3 Correlation of TOI% with systolic BP and eGFR TOI%, upper pole TOI%, lower pole Other variables r P-value r P-value eGFR −0.24 0.22 −0.30 0.11 Systolic BP 0.50 <0.01 0.45 0.01 TOI%, upper pole TOI%, lower pole Other variables r P-value r P-value eGFR −0.24 0.22 −0.30 0.11 Systolic BP 0.50 <0.01 0.45 0.01 BP, blood pressure. DISCUSSION This study demonstrates the feasibility of using NIRS to monitor kidney transplant perfusion in paediatric recipients. A significant correlation was observed between real-time NIRS TOI% and RI derived from the gold standard clinical measure of perfusion, DUS. Moreover, TOI% correlated with systolic blood pressure, a classic haemodynamic parameter related to allograft perfusion. The physiological principle underlying NIRS is that detection of a change in the spectrum of infrared light reflected from a tissue bed is dependent on the relative concentration of oxygenated and deoxygenated haemoglobin . The use of NIRS in perioperative and critical care has grown in recent years; the real-time continuous nature of monitoring and its ability to predict hypoxia-induced tissue damage in shocked patients earlier than gold standards of global perfusion such as blood pressure, lactate and the venous saturation of oxygen are considered its major advantages [21, 28]. Renal oxygen saturation was a reliable predictor of hypoxia-induced adverse outcomes, including acute kidney injury following cardiac surgery, and was demonstrated to be a superior marker of acute renal hypoperfusion than plasma creatinine, eGFR and urinary NGAL [21, 29]. A decrease in renal oximetry perioperatively or in states of shock is thought to reflect the shift of blood flow to the vital organs at the expense of kidney perfusion . DUS is considered the gold standard tool for assessing renal allograft perfusion; RI is an index of organ vascular compliance and correlates with eGFR in the early post-transplantation period and with long-term allograft survival [13, 18, 30, 31]. In this cohort of stable paediatric kidney transplant recipients, RI values were within the normal range reported in adult studies and no vascular complications were detected on DUS . An inverse relationship between NIRS TOI% and RI measurements was observed. This observation is physiologically plausible, as an increased RI represents higher vascular resistance that negatively impacts perfusion and organ oxygenation. These data corroborate previous observations in limb blood flow with agreement between NIRS and DUS . Vidal et al.  demonstrated that renal oximetry (NIRS) parameters tended to improve over the initial 3 days following transplantation, as a result of ongoing vascular remodelling, and correlated with graft function. The present study demonstrates that renal oximetry is associated with sonographic markers of perfusion under stable conditions. The utility of renal oximetry as a tool to monitor transplant kidney perfusion is reinforced by our observation that TOI% is directly correlated with systolic blood pressure, a traditional haemodynamic parameter. This suggests that NIRS could differentiate primary graft dysfunction caused by problems in organ perfusion in real-time arising either from surgical vascular complications (transplant renal vein or artery thrombosis), suboptimal circulatory volume or systemic blood pressure and thus kidney perfusion pressure. Paediatric kidney transplantation poses fluid management dilemmas. When an adult kidney is transplanted into a small recipient, large volumes of intravenous fluid and inotropes are used to ensure allograft perfusion, both of which can result in adverse effects if not implemented judiciously . Moreover, fluid management strategies are decided on clinical and biochemical indices of fluid status that are neither sensitive nor specific enough to recognize hypovolaemia or organ hypoperfusion . The diversity among various institutional post-operative fluid management protocols reflects these difficulties. Application of real-time perfusion monitoring with NIRS has the potential to overcome these challenges in the post-operative period. Decisions on the rate of intravenous fluid administration and inotrope use, currently based solely on clinical assessment, could be assisted by utilization of changes in NIRS parameters. A further potential application of NIRS in the early post-transplantation period is estimation of oxygen adequacy at a microvascular level. The sensitivity of DUS to detect cortical blood flow beyond arcuate vessels is limited, which impairs detection of early renal venous thrombosis and intrarenal vessel involvement [34, 35]. Moreover, DUS-derived RI is confounded by processes causing interstitial oedema in the transplant, such as rejection or acute tubular necrosis . Renal oximetry values in children with delayed graft function are similar to those from recipients with good function, supporting the value of NIRS in differentiating perfusion-related causes of graft dysfunction . Moreover, in experimental studies on rat kidneys, occlusion of the renal artery and vein resulted in a significant decline in renal oxygen saturation within a few seconds, with earlier detection than with clinical, laboratory or DUS assessment [37, 38]. No study to date has evaluated normal renal NIRS values in renal transplant recipients. Intraindividual variability is a key limitation of this technique, underlying the importance of trend monitoring rather than isolated absolute measurements [21, 39]. Renal NIRS TOI% values observed in our cohort are in accordance with values quoted from studies on native kidneys and from children in the early post-transplant period. Somatic NIRS values obtained from native kidneys are higher than cerebral by 10–20% and it has been suggested that a 20% decrease from baseline represents clinically significant hypoperfusion. This has led some investigators to propose that NIRS could be used in post operative patients to guide fluid management decisions. In a study that evaluated NIRS use in neonates after digestive surgeries, tailoring of the fluid management strategy based on NIRS measurements led to improved renal oximetry values, with the conclusion that regional renal oximetry reflects global perfusion status . NIRS tissue oxygen saturation has previously been reported to be affected by the distance of the organ of interest from the skin . Some investigators have proposed a maximum depth of 8 cm for use of this modality . In the current study, despite differing depths of the sampling sites from the skin, no significant difference in TOI% between the upper and lower poles of the transplant was observed. Furthermore, the effect of the interaction between TOI% and the poles’ distance from the skin was not significant. This supports the feasibility of NIRS monitoring across patients of different age, body habitus and surgical approach for allograft placement. When we conducted our analysis separately for patients with either intra- or extraperitoneally placed organs there was no difference in the allografts’ pole distance from the skin or in the TOI%. This observation is particularly important for the youngest recipients, who are more likely to have an intraperitoneally placed kidney. It is also noteworthy that measurements of renal oximetry from two different graft sites in our group of established paediatric renal transplant recipients are seemingly reproducible. Reproducibility of NIRS measurements can be enhanced with the use of two different channels for monitoring . In our study, we used two pairs of optodes (one for each graft pole) under a steady perfusion state. TOI% recordings were similar between the two poles in organs with homogeneity in perfusion according to DUS. Our study is limited primarily by the small number of participants. Its observational nature did not allow validation of the NIRS response versus DUS in situations where fluctuations in renal allograft perfusion take place. In the absence of NIRS normative data, the inherent method limitations in obtaining such and the importance of trend monitoring perioperatively, it becomes clear that renal oximetry needs further validation before it can be implemented in paediatric kidney transplantation. In order to validate our findings, a future observational trial where NIRS monitoring would start in the recovery area outside the operating room might be useful. It is common clinical practice that renal allograft perfusion is assessed immediately postoperatively with DUS. At this point, paediatric kidney recipients might have received up to 190 mL/kg intravenous fluid volume and potentially inotropes to maintain central venous pressure and optimal organ perfusion . NIRS indices at this point of optimized perfusion could be used as baseline values for the individual recipient–graft pair. Owens et al.  found that acute kidney injury in infants after cardiac surgery was predicted by a sustained decrease in renal oximetry values of >50% from baseline over 2 h. While this might be an excessive and unacceptably prolonged decline in the setting of kidney transplantation, previous studies have highlighted the importance of trend monitoring [21, 40]. It has been suggested that a 20–25% decline in renal oximetry was an AKI predictor in paediatric cardiac surgery and could prompt fluid resuscitation in neonates following digestive surgery [21, 40]. In order to establish which deviation from the baseline NIRS value obtained in the recovery room is clinically significant, data from NIRS recordings obtained over a 24-h period post-transplant could be incorporated into a receiver operating characteristics analysis aimed at assessing the depth and duration of renal tissue hypoxia that could best predict adverse outcomes in blood pressure, urine output and eGFR. Also, the impact of interventions such as administration of fluid boluses, diuretics and inotropes on NIRS parameters should be recorded and correlated to the respective changes in haemodynamic indices and allograft function. In summary, the current pilot study demonstrates the feasibility and tolerability of NIRS measurements in paediatric kidney transplantation. Real-time NIRS parameters correlate with DUS and systolic blood pressure as traditional measures of allograft perfusion. The depth of the transplant does not appear to influence NIRS accuracy. Further trials are warranted to examine the utility of NIRS for early recognition of microvascular events and to guide immediate decisions on fluid and inotrope management at the bedside in paediatric kidney transplant recipients. ACKNOWLEDGEMENTS This project was supported by the National Institute for Health Research (NiHR) Biomedical Research Centres based at Guy's and St Thomas National Health Service (NHS) Foundation Trust and King's College London as well as Great Ormond Street Hospital for Children NHS Foundation Trust and University College London. The views expressed are those of the authors and not necessarily those of the NHS, the NiHR of the Department of Health. AUTHORS’ CONTRIBUTIONS G.M., S.D.M., N.M., J.M. and W.N.H. designed the study. G.M., F.W., M.T-A. and T.W. collected the data. G.M. analysed the data. G.M. drafted and W.N.H. edited the manuscript. The results presented have not been published previously in whole or part, except in abstract form. CONFLICT OF INTEREST STATEMENT None declared. REFERENCES 1 Czyzewski L , Sanko RJ , Wyzgal J et al. Assessment of health-related quality of life of patients after kidney transplantation in comparison with hemodialysis and peritoneal dialysis . 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Nephrology Dialysis Transplantation – Oxford University Press
Published: Oct 1, 2018
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