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Saudi Journal of Kidney Diseases and Transplantation
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Year : 2012  |  Volume : 23  |  Issue : 5  |  Page : 985-992
Value of renal resistive index as an early marker of diabetic nephropathy in children with type-1 diabetes mellitus

1 Department of Pediatrics, Zagazig University, Zagazig, Egypt
2 Department of Radiodiagnosis, Zagazig University, Zagazig, Egypt

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Date of Web Publication13-Sep-2012


Constant increase in the incidence of type-1 diabetes (T1-DM) has made it necessary to have new markers for the early detection of diabetic nephropathy (DN). One of the markers that could be helpful in detecting functional alterations in renal hemodynamics is assessment of the renal resistive index (RI) by using renal Doppler. We studied 25 patients with T1-DM (Group-A), which comprised of 15 females and 10 males, with a mean age of 10.8 ± 2.2 years and duration of diabetes of 5 ± 1.1 years. A control group (Group-B) comprising 20 healthy children, 12 females and eight males with mean age of 11.6 ± 2 years, was also studied. The following parameters were studied in the two groups: age, serum creatinine, albumin excretion rate (AER), glomerular filtration rate (GFR), glycosylated hemoglobin (HbA1c) and mean renal RI of both kidneys. We found an increase in the mean RI in diabetic patients versus healthy children; the mean RI in Group-A was 0.64 ± 0.55 while it was 0.58 ± 0.0.28 in Group-B (P <0.000). This increase in RI had a positive correlation with duration of the disease, GFR and HbA1c levels, but there was no correlation with serum creatinine or AER. We conclude that RI is increased early in TI-DM, and it can be a predictor of DN.

How to cite this article:
Youssef DM, Fawzy FM. Value of renal resistive index as an early marker of diabetic nephropathy in children with type-1 diabetes mellitus. Saudi J Kidney Dis Transpl 2012;23:985-92

How to cite this URL:
Youssef DM, Fawzy FM. Value of renal resistive index as an early marker of diabetic nephropathy in children with type-1 diabetes mellitus. Saudi J Kidney Dis Transpl [serial online] 2012 [cited 2022 Jan 26];23:985-92. Available from: https://www.sjkdt.org/text.asp?2012/23/5/985/100880

   Introduction Top

Over the last decade, the incidence of childhood-onset type-1 diabetes mellitus (T1-DM) has significantly increased, particularly in children under the age of five years. [1] Diabetic nephropathy (DN) is defined as persistent proteinuria greater than 500 mg/24 h, or albuminuria greater than 300 mg/24 h. [2] DN remains the leading cause of end-stage renal disease (ESRD) in the Western world, responsible for nearly half of all new ESRD cases in the USA. [3] However, only a minority of patients with T1-DM progress to ESRD. [1] Although overt DN is rarely seen in children with type-1 or type-2 diabetes, in less than 1% of the pediatric population, [4] early structural and functional renal alterations develop soon after diagnosis in children and accelerate during puberty. [3]

All patients with T1-DM appear to develop structural changes of diabetes in the glomerulus, some very slowly and others so fast as to result in overt DN in as little as ten years. Glomerular lesions are present in patients with T1-DM before the onset of the clinical manifestations of DN. [5]

Doppler sonography may be a useful comple mentary test in the evaluation of DN, even in the early stages. [6] Early stage of vascular involvement seems, in fact, to be characterized by functional alterations of endothelial control on vascular tone and wall interaction with circulating cells. Renal Doppler assessment of RI is a reliable, non-invasive evaluation of arterial function and is particularly useful for early diagnosis of vascular involvement. [7] In DN, the natural pathways to renal insufficiency pass through a phase of normal albumin excretion rate (AER) with high glomerular filtration rate (GFR) to a phase of high AER with normal GFR, followed by high levels of AER with reduced GFR. [8] Increasing evidence suggests that the intra-renal arterial RI, measured by Doppler ultrasound, a well-established technique for the investigation of renal morphology and hemodynamics, predicts the course of renal function in several conditions. No standard, validated, cut-off to distinguish normal from high RI has been identified to date. RI values between 0.75 and 0.85 have been associated with renal functional impairment in patients with chronic kidney disease and stenosis of the renal artery, and they also predict allograft dysfunction in kidney transplant recipients. Little information is available on the use of RI for the identification and prediction of DN in routine clinical practice. It is yet unclear whether RI predicts DN in low-risk patients; also, the correlation between increased intra-renal RI and altered renal hemodynamics remains unclear independent of albuminuria, as also the most appropriate cut-off value. [9],[10]

   Objectives Top

The objective of this study was to evaluate the renal RI in children with T1-DM and to compare the values with normal healthy children and analyze whether it would help to predict early DN.

   Patients and Methods Top

The study was designed as a case control cross-sectional observational study; we studied 25 cases with T1-DM (Group-A) and 20 age-matched healthy children who served as the control group (Group-B).

There were 15 females and 10 males in Group A having a mean age of 10.8 ± 2.2 years (7-15 years); the duration of diabetes was 5 ± 1.1 years (3.5-7 years) with confidence interval (CI) at 95% (4.5-5.5). Group-B comprised of 20 healthy children, including 12 females and eight males with a mean age of 11.6 ± 2 years (8-15 years). Patients with a known history of renal disease, serum creatinine >1.3 mg/dL or GFR <60 mL/min/1.73 m 2 , or those who had any medical disease other than diabetes, were excluded.

The study was performed at the Department of Pediatrics and Radio-diagnosis, the Zagazig University Hospital, in the period from September 2009 to January 2010. In all patients, a thorough review of their medical files and detailed clinical examination, including measurement of blood pressure (BP), was undertaken. Also, all investigations performed on these patients in the past three months were reviewed and the following tests were performed: serum creatinine, glycosylated hemoglobin (HbA1c), urine examination for AER and assessment of GFR. Lastly, we performed renal Doppler at the Radiology Department.

HbA1c assay

The mean value of three consecutive measurements of HbA1c was considered representative of metabolic control. The HbA1c was analyzed by HPLC (variant II, Bio-Rad), with the normal range being 4.5-6.5%.

Microalbuminuria (MA) assay

Urinary albumin excretion was measured with radioimmunoassay (Albumin DA; Sclavo, Siena, Italy) in 24-h urine collections; urinary AER lower than 30 mg/24 h was considered normal, whereas AER of 30-300 mg/24 h was considered indicative of MA. [1]

GFR assay

Creatinine clearance was determined from a 24-h urine collection. It is one of the most useful clinical estimates of GFR, which is defined as the volume of plasma that is cleared of creatinine by the kidney per unit of time. It was calculated using the following formula:

Creatinine clearance = U creat conc x V / P creat conc

The normal range for GFR in our laboratory is 80-130 mL/min/1.73 m 2 . Patients were considered to have a hyper-filtering kidney when the GFR was higher than 130 mL/min/1.73 m 2 (higher limit of normal).

Renal RI

Resistance to blood flow can be quantified by measuring the RI, which is calculated using the following formula:

RI = (peak systolic velocity - end diastolic velocity) / peak systolic velocity.

All selected cases were subjected to B-mode ultrasonographic examination of both kidneys for assessment of the renal size, shape and echogenicity and to exclude other renal diseases. Also, color Doppler ultrasonography examination of the intra-renal arteries was performed using a 3.5 MHZ convex transducer (Toshiba Nemio Medical System).

Children were evaluated in the prone position after approximately three hours of fasting. The Doppler sample volume was positioned after color positioning of the inter-lobar arteries. Low wall filter was used and all waveforms were measured on the largest Doppler scale by using the minimum pulse repetition frequency that does not produce aliasing. The angle of transducer was set to obtain maximum waveform amplitude and clarity. Three successive cardiac cycles (of each vessel) were recorded. Maximum systolic and diastolic velocities were selected manually and the RI was then calculated using integrated software of the ultrasound unit. RI of the three waveforms of three vessels in different sites (upper, middle and lower zones) was obtained. Following this, the mean value for each kidney was calculated. The left and right kidneys had similar patterns and data in each patient. All the Doppler examinations were performed by the same examiner to avoid inter-observer variability. A normal RI is below 0.7 in adults and children who are six years of age or older. [11]

   Statistical Analysis Top

Statistical analysis was performed using a computer-based program (SPSS version 11). The quantitave data are presented as mean ± standard deviation. Unpaired independent t test is the statistical test of significance for the two groups. P-value less than 0.05 indicated statistical significance. Pearson correlation was done to express the correlation between the two parameters.

   Results Top

There was a significant increase in HbA1c, GFR and mean renal RI in Group-A patients when compared with Group-B; P < 0.05 [Table 1]. No significant difference was seen in the age, serum creatinine or AER between the two groups; P >0.05.

[Figure 1] shows the range of mean RI in Group-A and Group-B patients. [Figure 2] shows a nine-year-old child from Group-B with RI in the right kidney of 0.55 and [Figure 3] shows an 11-year-old child with T1-DM for seven years, with RI in the left kidney of 0.75.
Figure 1: The range of the mean resistive index in patients in Group-A and Group-B.

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Figure 2: A nine-year-old child from Group-B with right kidney resistive index of 0.55.

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Figure 3: An 11-year-old child with type-1 diabetes mellitus for 7 years with left kidney resistive index of 0.75.

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[Table 2] shows a negative correlation between mean renal RI and age, positive correlation between mean RI and duration of disease and positive correlation between HbA1c and GFR, while there was no correlation between mean renal RI and serum creatinine or AER.

[Figure 4] shows the correlation between different parameters and mean RI; [Figure 4]a shows a positive correlation between duration of the disease and mean RI, [Figure 4]b shows a positive correlation between HbA1c and mean RI, [Figure 4]c shows a positive correlation between GFR and mean RI and [Figure 4]d shows lack of correlation between AER and mean RI.
Figure 4: Correlation between different parameters and mean resistive index (RI); (a) shows positive correlation between duration of disease and mean RI, (b) shows positive correlation between glycosylated hemoglobin and mean RI, (c) shows positive correlation between glomerular filtration rate and mean RI, (d) shows no correlation between albumin excretion rate and mean RI.

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   Discussion Top

Many authors have suggested that studying the clinical and renal functional as well as renal structural parameters can improve the predictive capability of albuminuria for progresssion of DN. [12] The knowledge developed in adult pathology cannot be systematically applied to children whose renovascular physiology is different. [13]

There is no general agreement about the meaning and the predictive value of renal RI in patients with DN. Only a few studies describing the application of Doppler sonography in evaluation of intra-renal hemodynamic abnormalities in DN have been published so far, and most of these were performed in adults with type-1 or type-2 diabetes mellitus. [10]

In this study, the mean age of the patients was 10.8 ± 2.2 years and the mean duration of diabetes was 5 ± 1.1 years. We found no significant increase in AER in the patient-group over the control-group. This can be explained by the observation that the maximum incidence of MA occurs 15 years after the onset of diabetes. [14] Also, most of the study children had onset of T1-DM before puberty; it has been shown that patients who have T1-DM from early childhood, and especially those diagnosed under five years of age, seem to have a slightly delayed onset of persistent MA during the first ten to 15 years of their diabetes duration when compared with patients diagnosed later in childhood or during puberty. [15] MA is rare before puberty, even in diabetics of long duration. [16]

In the current study, there was an increase in GFR in the patient-group (140.6 ± 9.3 mL/ min/1.73 m [2]) in comparison with the control-group (113.9 ± 15.6 mL/min/1.73 m 2 ); P <0.05. It is important to detect this increase in GFR because recent studies suggest a direct link between hyperfiltration and subsequent progresssive decline in GFR. [18] In our study, we found that hyperfiltration state can be detected earlier than the stage of MA. This is in accordance with Gross et al, who described that MA was found to be an independent predictor of hyperfiltration stage and that increased albumin excretion in T1-DM nephropathy was found in a more advanced stage than glomerular hyperfiltration. [2]

The patients in Group-A had a higher HbA1c (8.9 ± 0.8%) than those in Group-B (5.2 ± 0.57%); this level is higher than the recommended target HbA1c level of less than 7.5% [National Institute of Clinical Excellence (2004), [17] and Australasian Pediatric Endocrine Group (2005)]. [18] Surveys of glycemic control have consistently demonstrated similarly poor control in other regions: the mean HbA1c level was 8.8% in Asia and the Western Pacific Region, [19] 8.3% in the Hvidore study (Mortensen and Hougaard, 1997), [20] 8.2% in New South Wales, Australia Craig et al, 2002, [20] 8.7% in Scotland (Scottish Study Group for the Care of the Young Diabetic), 2001, [21] and 9.0% in France, Rosilio et al, 1998. [22] This could be because not all children with T1-DM in our area monitor blood glucose levels regularly at home, which in turn could be due to monetary reasons.

In this study, we found a significant increase in the mean renal RI in children with T1-DM over age-matched healthy children [0.64 ± 0.55 (0.54-0.75) versus 0.58 ± 0.28 (0.54- 0.63)]; P <0.05. This is in accordance with the findings of Soldo et al [23] and Frauchiger et al, [24] who found that the RI has been advocated as a useful marker of DN. Recently, however, Okten et al reported that renal Doppler sonography was not useful for the prediction and early detection of DN in children, [25] while Sperandeo et al suggested that duplex Doppler sonography may be a useful complementary test in the evaluation of DN, even in the early stages. [6] The determination of renal size and renal parenchymal echogenicity proved to be of little value. The most relevant clinical information is provided by the RI, a parameter that will allow the early detection of patients affected by type-2 DM, who show renal vascular involvement without any alterations of the traditional ultrasound parameters. [26] Raes et al explained this increase in RI by an increase in the diastolic blood pressure during exercise, suggesting that renal functional abnormalities may be partly explained by a systemic vasculopathy, which is also present in the kidney. [27] However, other studies have suggested that Doppler sonography offers little extra beyond serum creatinine levels and creatinine clearance rates in patients with early DN and normal renal function. [28],[29],[15],[30]

We found a negative correlation between age and mean RI; this is in accordance with Dacher who reported that the RI is higher in infants (0.7-0.8) than in children and adults (0.55-0.6). [13] In our study, there was a positive correlation between the duration of diabetes and mean RI. Multiple regression analysis revealed that the RI values in patients with DM were significantly affected by creatinine clearance, age and duration of type-2 diabetes. [31]

We found a positive correlation between HbA1c and mean RI. There are reports suggesting a general decreasing incidence of diabetic vascular complications related to improved and more intensive insulin treatment, resulting in better quality of diabetes care. This might, at least, lead to less severe complications in the future. [15]

There was a positive correlation between GFR and mean RI in our study, which matched the findings of Okten et al, [25] who found that both RI and renal volume showed correlation with GFR. [10] However, this is in contrast to Marzano et al, who found a statistically significant negative correlation between radioisotope evaluation of GFR and the RI of inter-lobar arteries. [28] The presence of a very low RI at the level of the inter-lobar arteries in patients with T1-DM was first described by Platt et al, [32] who observed a mean RI of 0.52 ± 0.05 in a group of 13 diabetic patients suspected to have hyperfiltering kidneys with normal creatinine levels and creatinine clearance greater than 130 mL/mm. An RI value lower than 0.5 is highly specific (98%) and has a high positive predictive value (90%) in the diagnosis of glomerular hyperfiltration. However, RI of less than 0.5 has a low diagnostic sensitivity (25%). We can speculate that Doppler ultrasound can help identify only a subset of patients with hyperfiltering kidneys in whom such hemodynamic changes are more pronounced. Because of their low diagnostic sensitivity, these Doppler parameters cannot replace radioisotope evaluation of GFR in the screening of glomerular hyperfiltration. [14] Our results disagree with the findings of Okten et al, who found that the mean RI value was not different in patients with glomerular hyperfiltration compared with patients with a normal filtration rate. [25]

There was no correlation between AER and the mean RI in our study, which is in agreement with some other studies. [25] In type-2 DM also, Baris et al found no relationship between renal RI and AER. This might indicate that intra-renal impedance is not influenced by glomerulopathy, which is the main mechanism responsible for AER in diabetic patients. [33]

We conclude that renal RI increases in children with T1-DM, which positively correlated with age, duration of disease, HbA1c and GFR, and was independent of AER. Thus, renal RI can be used as an early predictor of DN. We recommend more studies on a larger sample size to confirm our findings.

   References Top

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31.Ishimura E, Nishizawa Y, Kawagishi T, et al. Intrarenal hemodynamic abnormalities in diabetic nephropathy measured by duplex Doppler sonography. Kidney Int 1997;51: 1920-7.  Back to cited text no. 31
32.Naroei M, Jafari B, Alipour P. Arterial Resistive Index (RI) in Type II Diabetic Nephropathy Stages and Healthy Controls. Iran J Radiol 2009;6:29-32.  Back to cited text no. 32
33.Afsar B, Elsurer R, Sezer S, Ozdemir FN. Insulin resistance is associated with increased renal resistive index independent of other factors in newly diagnosed type 2 diabetes mellitus and hypertensive patients. Metabolism 2010;59:279-84.  Back to cited text no. 33

Correspondence Address:
Doaa Mohammed Youssef
Lecturer of Pediatrics, Department of Pediatrics, Zagazig University, Zagazig
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DOI: 10.4103/1319-2442.100880

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1], [Table 2]

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