|Year : 2019 | Volume
| Issue : 1 | Page : 1-8
Renal duplex ultrasonography among adult native Nigerian diabetics and diabetic nephropathy population
Sarah Sunday Assenyi1, Ademola Joseph Adekanmi2, Aarinola Esan3
1 Department of Medicine, College of Medicine, University of Ibadan, Ibadan, Nigeria
2 Department of Radiology, College of Medicine, University of Ibadan, Ibadan, Nigeria
3 Division of Endocrinology, Department of Medicine, University College Hospital, Ibadan, Nigeria
|Date of Web Publication||28-Dec-2018|
Dr. Ademola Joseph Adekanmi
Department of Radiology, College of Medicine, University of Ibadan, Ibadan
Background: Diabetes mellitus (DM) is a serious global health problem with grave socioeconomic impact and debilitating complications especially diabetic nephropathy (DN). This study evaluated the usefulness of renal parenchymal and vascular sonography among three groups-diabetics with nephropathy, diabetes with no evidence of nephropathy and nondiabetics.
Materials and Methods: The renal volume, parenchymal changes, and intrarenal vascular indices of three groups of participants (Group A - Diabetic with nephropathy; Group B - diabetic without nephropathy; and Group C - nondiabetic controls) were assessed using B-mode and Duplex ultrasonography.
Results: The difference in the means of resistance index (RI) and pulsatility index (PI) in the diabetic patients (Group A and Group B) was significantly higher compared to the controls (RI mean ± standard deviation [SD]: Group A diabetic patients, 0.71 ± 0.11 cm3; Group B diabetics, 0.68 ± 0.08 cm3; controls, 0.62 ± 0.07 cm3; P < 0.0001); (PI ± SD: Group A diabetic patients, 1.22 ± 0.25 cm3; Group B diabetics, 1.16 ± 0.29 cm3; controls, 1.03 ± 0.23 cm3; P = 0.003). The mean renal volume among DM patients (Group A and Group B) were higher than in nondiabetic controls, (mean renal volume ± SD: Group A DM patients with nephropathy, 13.99 ± 3.95 cm3, the diabetic group without DM patients 13.39 ± 4.59 cm3, controls 12.05 ± 3.39 cm3).
Conclusion: This study showed that renal RI and PI were significantly increased in patients with diabetes than in healthy controls with a trend of increase from controls to DM without nephropathy to DM with nephropathy. Duplex ultrasonography is useful for the clinical evaluation of diabetes and DN.
13.95 + 7.02% VS 8.20 + 4.19% P = 0.000
Keywords: Diabetes mellitus, diabetic nephropathy, pulsatility index, renal volume, resistivity index, ultrasonography
|How to cite this article:|
Assenyi SS, Adekanmi AJ, Esan A. Renal duplex ultrasonography among adult native Nigerian diabetics and diabetic nephropathy population. West Afr J Radiol 2019;26:1-8
|How to cite this URL:|
Assenyi SS, Adekanmi AJ, Esan A. Renal duplex ultrasonography among adult native Nigerian diabetics and diabetic nephropathy population. West Afr J Radiol [serial online] 2019 [cited 2019 May 26];26:1-8. Available from: http://www.wajradiology.org/text.asp?2019/26/1/1/248957
| Introduction|| |
Diabetes is a serious health problem with great socioeconomic impact on the health-care system throughout the world. According to the World Health Organization (WHO) projection, about 221 million people were affected by Diabetes in 2010, 382 million people in 2013; the number is expected to increase to a staggering 300 million people globally by 2025 and 592 million in 2035. In Africa, the International Diabetes Federation estimates that over 5 million people suffer from the disease and the number is expected to increase to 15 million by 2025. Nigeria is documented to have the greatest number of people living with diabetes in Africa compared to over four decades ago which showed low prevalence rates of less 1%; the current prevalence of diabetes mellitus (DM) in Nigeria is not known but estimated at 10%. As the incidence of diabetes in the African population increases, the incidence of diabetic complications is also increasing correspondingly., This has resulted in major health-care issues and enormous economic burden, particularly in poor African countries grappling with the scourge of various infectious diseases, from the direct cost of intensive monitoring and control of the disease and the long-term management of the cardiovascular, renal, ophthalmic, and neurological complication.
Renal changes in DM include diabetic nephropathy (DN) from infectious, parenchymatous, and vascular lesions; microvascular lesions resulting in glomerulosclerosis and macrovascular lesions resulting in renal arteriosclerosis., According to the annual report of the Japan Dialysis Treatment Society in 2006 and a study by Pamela A. Carmines, diabetes is documented as the most frequent cause of end-stage renal disease. Milovanceva-Popovska and Dzikova reported that renal changes could be assessed using duplex ultrasound scan (USS). Medical Ultrasound is noninvasive, affordable, and available, it is free of ionizing radiation and is an early predictor of the advanced stage of DN.,
There have been various studies in Greece, Denmark, and Saudi Arabia,, on renal parenchyma and/or vascular changes in diabetic patients; however, data on renal size/volume, parenchyma, and Doppler vascular changes among persons with diabetes in Nigeria are suboptimal. This study, therefore, aims to determine the findings of Duplex USS in the evaluation of renal parenchymal and vascular abnormalities and to correlate these changes with clinical and laboratory parameters.
| Materials and Methods|| |
Study design and study population
This was a comparative cross-sectional study among adults with type 2 diabetic patients in one of the foremost regional, referral tertiary Health institution in West Africa. The target population was adult type 2 DM patients attending or referred to the Endocrinology clinic of the University College Hospital (UCH), Ibadan.
Study site and setting
This study was conducted jointly at the Medical Outpatient clinic and the Ultrasound suite of the Department of Radiology of UCH, Ibadan. UCH is a tertiary referral hospital located in Ibadan, South-West Nigeria. UCH, Ibadan has facilities for specialist care for diabetics and ultrasonography.
Sample size determination
The sample size was estimated using the formula for a comparison of mean between two groups. The desired power and level of statistical significance for this study was set at 90% and 5%, respectively. After adjusting for 10% nonresponders, the minimum sample size was 46. The sample size was 138 (i.e., 46 participants with DN, 46 participants without DN, and 46 controls).
A purposive sampling technique was used to select all consenting participants.
Adults more than 18 years of age. Cases were those that met the definition of diabetes as defined by the WHO., The enrolled DM patients were grouped based on their glomerular filtration rate (GFR) into two groups: (i) Group A - Diabetic with nephropathy (DN) and (ii) Group B - Diabetes only (DMo), i.e., DM without nephropathy. While Group C was apparently healthy normotensive adult controls without symptoms referable to diabetes, renal or vascular diseases, who have normal blood glucose levels.
Those who declined consent were excluded from the study but will receive standard level of care as per the National guideline. All diabetics below the age of 18 years and those patients with baseline renal disease.
Ethical approval was obtained from the UI/UCH Ethical Review Committee. Informed consent was gotten from all patients. Their participation was voluntary; subjects had the right to withdraw from the study without jeopardizing their standardized care. Confidentiality was ensured by assigning participants' data numerical values instead of real names. All data were kept in a safe place.
Data collection, instrument, and quality controls
The clinical parameters of all consenting patients including measurement of blood pressure to calculate their mean arterial blood pressure (MAP), weight, and height were recorded, and their body mass index (BMI) calculated; plasma urea and creatinine levels, as well as the blood sugar levels, serum creatinine, and lipid profile values, were also documented. DM was confirmed with fasting blood sugar (FBS) ≥126 mg/dL or postprandial blood sugar (PPBS) ≥200 mg/dL on two occasions. Laboratory values of serum creatinine, 24-h urine protein (mg/dL) and the estimated GFR (eGFR) were calculated for all diabetic cases. According to the Chronic Kidney Disease Epidemiology Collaboration eGFR formula, diabetics were grouped into DN and diabetes without nephropathy (DMo) according to the guidelines (i.e., eGFR < or >60 mL/min/1.73 m2).,
Relevant sociodemographic data and details of risk factors, as well as other clinical and laboratory data of each participant, were recorded in the prepared data form.
USS was performed using a General Electric Logic P5 ultrasound scanner with Doppler facilities. The participants were scanned with a transabdominal pulsed, 2–5 MHz curved transducer in a supine position after an overnight fast and during suspended respiration at inspiration. B-mode scanning was used to locate the kidneys in a sagittal scan at the flanks, and the parenchyma findings were documented as; normal, decreased, or increased. Other parenchymal findings such as cortical cysts were also documented. The craniocaudal length, the anteroposterior height and the width of the kidneys were also measured and recorded. The renal volumes were calculated using the ellipsoid formula (length × height × width × 0.52). Thereafter, Doppler USS (DUS) of the intra-renal vessels at the level of the interlobar arteries was carried out. For DUS, wall filter was set to the minimum (50 Hz) and the sample volume was set at 2–5 mm, and the resistance index (RI) and pulsatility index (PI) were measured and documented. The medications of the subjects were continued during this study.
All the Doppler examinations were performed by the same examiner (a qualified radiologist) to avoid interobserver variability. The RIs and PIs for each kidney and the mean RI and PI values were also obtained for each patient by averaging the mean RI and PI values of the two kidneys; after three values had been obtained. These values were recorded on the ultrasound data sheet.
The data generated were entered and analyzed using the statistical package for social sciences (SPSS) version 20.0 (SPSS, Chicago, IL, USA). Chi-square test was used to test association between qualitative variables while Student's t-test was used to test association between quantitative variables at 5% level of significance. The correlation between two variables was assessed by the Spearman coefficient. Categorical data were expressed as percentages. The Chi-square or Fisher's exact test was applied as appropriate.
| Results|| |
A total of 138 individuals participated in this study comprising of 92 patients diagnosed with diabetes and 46 participants without diabetes (controls). Forty-six of the diabetics had nephropathy. The mean age of the individuals in the DM group was 59.32 ± 10.43 years with a range of 34–84 years, while mean age for controls was 58.04 ± 9.46 years (Range = 38–80 years). About 39.1% of the controls were males while among the diabetics, 32.6% were males; 60.9% of the controls were females while among the diabetics, 67.4% were females. Among the diabetics, the mean age of DM patients without nephropathy was 57.84 ± 11.14 years while the mean age of DM patients with nephropathy was 63.13 ± 9.27 years.
Clinical parameters of the study population
The difference in mean of the Mean arterial blood pressure (MAP) among DN (97.76 ± 16.01 mmHg), DMo (91.64 ± 10.66), and control (84.04 ± 5.37) were statistically significant (P < 0.001). Pairwise comparison showed that the mean of the MAP of DN and DMo were statistically significantly higher than MAP of controls. Furthermore, the MAP for DN was higher than in DM, but this was not statistically significant. However, there was no significant difference in the mean values of the BMI of the individuals in the three groups.
The duration of DM was not statistically significantly higher in the DN than DMo [Table 1].
|Table 1: Clinico-laboratory parameters of the diabetics with/without nephropathy and the controls|
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Laboratory parameters of the diabetic group and the controls
As shown in [Table 1], the mean of the serum creatinine level of DN patients (1.82 ± 0.56 mg/dL) was statistically significantly higher than the mean serum creatinine level of diabetic cases without nephropathy (0.84 ± 0.34) and the mean serum creatinine level of the controls (0.51 ± 0.49), respectively (P < 0.001). Furthermore, the mean serum creatinine level of diabetic cases without nephropathy was statistically significantly higher than the mean serum creatinine level of the controls.
The mean FBS level of DN patients (124.5 ± 21.04 mg/dL) and the mean FBS level of DMo (121.6 ± 30.54) each were statistically significantly higher than the mean FBS level of the controls (91.46 ± 15.80), respectively (P < 0.001). There was no statistically significant difference between the means of FBS level in DN and DMo. Similar pattern was seen in the mean HbA1c among the three groups [Table 1].
The high-density lipoprotein, low-density lipoprotein, triglycerides, and PPBS levels were all found to be higher in the DN, but the difference was not statistically significant. In addition, the 24-h urinary albumin showed no significant differences in their mean values among those with and without nephropathy [Table 1].
Renal ultrasonographic findings
B-mode and Doppler ultrasonography of 276 kidneys were evaluated in this study. On B-mode scans, the mean volume of the left kidney was greater than that of the right kidney in the three groups. There was a statistically significant difference in the mean of left renal volume among DN (13.99 ± 3.95 cm3), DMo (13.39 ± 4.59), and the controls (12.05 ± 3.39). DN patients had statistically significantly higher mean right renal volume than the controls. However, the mean right renal volume for control cases and diabetic cases without nephropathy, as well as the mean right renal volume of DN and DMo, respectively did not differ significantly [Table 2]. Abnormal parenchymal changes were detected only in five (6.9%) of the patients with diabetes (both DN and DMo): Two had increased echogenicity in both kidneys, one had decreased echogenicity of both kidneys, and the remaining two had increased echogenicity in the right kidneys only. The DN patients showed increased echogenicity in two individuals; this was seen in the right kidney in a subject, while both kidneys were involved in the other subject. Among the diabetic cases without nephropathy, increased echogenicity was also found in two patients; on the right and left kidney, respectively. While a patient had decreased echogenicity, no abnormal parenchymal findings were documented in the control group. Incidental renal parenchymal cortical cysts were detected in eight diabetic patients but none in the controls. Most (5/8) of the cysts observed were in diabetic cases without nephropathy group with 62.5% occurring in the right kidneys. No renal masses were seen in this study.
|Table 2: Differences in renal volumes and doppler parameters in the diabetics with/without nephropathy and the controls|
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Doppler interrogation of the interlobar renal arteries of the kidneys showed that difference in means of the RI in DN (0.71 ± 0.11), DMo (0.68 ± 0.08), and control (0.62 ± 0.07) were statistically significant, F (2133) = 11.06, P < 0.001. Post hoc test showed that the RI of both DN and DMO was statistically significantly higher than in control cases. However, the mean RI of DN patients and DMo did not differ significantly.
Likewise, the difference in mean of the PI among DN (1.22 ± 0.25), DMo (1.16 ± 0.29), and control (1.03 ± 0.23) was statistically significant (P = 0.003). Among the groups, patients with DN had statistically significantly higher mean PI than controls. However, when compared pairwise, the mean difference in PI for DN and DMo did not differ significantly [Table 2].
Correlation of renal-Doppler indices with risk factors for diabetes
The Spearman's Rho correlation analysis of the intrarenal Doppler RI with clinical risk factors of diabetes in both diabetic cases with or without nephropathy showed statistical significant correlations with age (r = 0.222, P = 0.035), and duration of diabetes (r = 0.351, P = 0.004) while the intrarenal Doppler PI showed statistical significant associations with age (r = 0.380, P < 0.001), duration of diabetes (r = 0.358, P = 0.003), cholesterol level (r = −0.209, P = 0.048), and serum creatinine (r = 0.222, P = 0.036) [Table 3]. Using the Student's t-test, there was no statistically significant difference in the means of both kidney RI and PI between male and female [Table 4].
|Table 3: Correlation of the intra renal doppler resistivity index and pulsatility index with clinical factors of diabetes among diabetic patients|
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|Table 4: Relationship between gender with diabetes mellitus and intra renal parameters|
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Factors associated with nephropathy among diabetic patients
There was the statistically significant difference in the mean age of DMo 56.96 ± 10.4 years and the mean age of DN 61.67 ± 9.88 years (P = 0.029, 95% confidence interval [CI] 0.49; 8.95). There was also statistical significant difference in the mean arterial blood pressure between DN 91.64 ± 10.66 mmHg and DMo 97.76 ± 16.02 mmHg (P = 0.034, 95% CI 0.49; 11.76) [Table 5].
|Table 5: Risk factors associated with nephropathy among diabetes mellitus patients|
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Predictors of diabetic nephropathy in the study population
After adjusting for confounders, intrarenal Doppler parameters (RI and PI) were not statistically significantly associated with nephropathy in DM. However, the MAP was statistically significantly associated with nephropathy in DM using logistic regression. A unit increase in MAP increases the risk of nephropathy in DM by 5% (odds ratio [OR] 1.05, 95% CI 1.01; 1.09, P = 0.015). Furthermore, female DM patients were about six times more likely to have nephropathy than male DM patients (OR = 5.68, 95% CI 1.09; 29.60, P = 0.039) [Table 6].
|Table 6: Multivariate analysis of nephropathy in diabetes mellitus patients and predictors|
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| Discussion|| |
DM if uncontrolled is associated with slow but relentless damage to the kidneys and virtually every organ in the body over time. A frequent microvascular complication of DM is DN, with early functional and structural abnormalities seen some few years after the onset of the disease. Our study indicates that intrarenal vascular resistive indices (RI and PI) and the mean renal volume, were higher in diabetic group compared to the controls; this is in agreement with the findings of other researchers.,,,,, Contrary to the study by Milovanceva-Popovska and Dzikova, intrarenal RI and PI were not statistically significantly associated with DN; this may be due to the smaller sample size employed and different study design in their study. In our study, age, duration of diabetes, and MAP showed a significant correlation to the intrarenal indices, but only age and MAP were significantly associated with DN.
We observed that left renal volumes were higher than the right in all the groups, which agrees with the work of Singh and Hoy and Saeed et al. This has been adduced to the smaller volume of the spleen compared to the liver on the right, allowing for larger growth of the left kidney. In addition, the shorter and straighter left renal artery with increased flow to the left kidney may contribute to its larger size. The slightly higher mean renal volumes in the Diabetic groups (DN and DMo) compared to the nondiabetic controls is in agreement with the reports of Brkljacić et al. This may be attributed to the diabetic kidney hypertrophy-hyperfiltration-hyperfunction syndrome from increased protein-DNA ratio to meet the highly filtrated components from the bloodstream. The lack of marked difference in renal volumes observed in this study may be because the studied DM patients have been on treatment for many years (mean duration of diabetes among DN = 12.7 years) thus slowing the expected diabetic renal changes over time.
There is no consensus on the significance of renal parenchymal hyperechogenicity as a reliable sign of renal functional impairment;, however, this study showed no relationship, in agreement with the reports of Baxter and Sidhu.
The RI and PI in the DM groups were significantly higher compared to the control group, probably due to renal damage at the glomeruli level and advanced arteriosclerosis in intrarenal arteries. On the other hand, only a slight insignificant increase in RI was seen in DN group when compared to DMo; this agrees with the findings of other researchers., We presumed that this may be because most of the cases of DN in this study were in the early stage of DN, as exemplified by the level of microalbuminuria recorded, although it was measured once in this study. This may also be due to good management of the DM cases with prevention of overt changes of DN. In this study, it was considered that RI values >0.70 and PI values >1.20 are indicative of renal impairment in type II diabetes in this environment, similar to studies by Platt et al. and Dawha et al. We observed that RI values had a relatively smaller coefficient of variance and standard deviation than PI values; thus, RI showed less variability in renal Doppler sonography. However, PI shows more intrarenal hemodynamic changes among the Diabetic population in this study, as reported by Koenhemsi et al. In previous studies,,, the diabetic patients with higher RI and PI values had a longer diabetes duration; likewise, this study shows a positive statistically significant correlation between the RI and the duration of diabetes. Unfortunately, there is paucity of literature on intrarenal PI in DM, thus limiting comparison with other studies. The RI and PI showed a significant direct relationship with the age and duration of diabetes, which could serve as an indicator of renal dysfunction in diabetic kidney disease., Our study showed that patients aged 60 years and above had higher RI and PI values, attributable to true renal dysfunction in senescent kidneys, rather than the higher values in the elderly solely due to misleading variations or an age-dependent variability in the RI,, as evidenced by correlations with compromised creatinine clearance in them, similar to studies by Radermacher et al. and Youssef and Fawzy Gender was not significantly related to the intrarenal Doppler parameters in this study. On the other hand, age and MAP showed a significant correlation with intrarenal RI; this is in accordance with studies by Pearce et al. as reported by Ishimura et al. and Milovanceva-Popovska and Dzikova. respectively. Age and MAP were the only factors that showed significant association with DN in this study. However, tests of association between RI and PI with DN showed that intrarenal Doppler RI and PI were not statistically significantly associated with DN contrary to the study by Milovanceva-Popovska and Dzikova, presumably due to the smaller sample size employed by them and differences in population dynamics of the participants among other factors.
Intrarenal RI and PI were not significant predictors of DN, but the mean arterial blood pressure and female gender were. A unit increase in mean arterial blood pressure was found to increase the risk of nephropathy in DM by 5% (OR = 1.05; 95% CI 1.01, 1.12; P = 0.022) in this study. Furthermore, female DM patients were about six times more likely to have nephropathy than male DM patients; however, more studies should be done to corroborate this finding.
| Conclusion|| |
In this study, we posit that Doppler vascular indices, PI and RI, are useful parameters in the assessment of intrarenal hemodynamic abnormalities present in DN and may contribute to early diagnosis and possible determination of the disease progression, although intrarenal PI was found to show more intrarenal hemodynamic changes than RI. Furthermore, renal parenchyma hyperechogenicity was not a reliable indicator of renal impairment in diabetics; however, subsequent research should be done to ascertain the role of medications on parenchymal changes. Furthermore, high MAP in diabetics significantly affects progression to DN.
We propose that renal vascular and parenchyma parameters, as well as urinary albumin/creatinine ratio, be measured routinely in diabetic patients.
The project described was supported by the Medical Education Partnership Initiative in Nigeria (MEPIN) project funded by Fogarty International Center, the Office of AIDS Research, and the National Human Genome Research Institute of the National Institute of Health, the Health Resources and Services Administration (HRSA) and the Office of the U.S. Global AIDS Coordinator under Award Number R24TW008878. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding organizations.
Financial support and sponsorship
This work was funded by the Medical Education Partnership Initiative in Nigeria (MEPIN) project funded by Fogarty International Center U.S.
Conflicts of interest
There are no conflicts of interest.
| References|| |
Kyari F, Tafida A, Sivasubramaniam S, Murthy GV, Peto T, Gilbert CE, et al.
Prevalence and risk factors for diabetes and diabetic retinopathy: Results from the Nigeria national blindness and visual impairment survey. BMC Public Health 2014;14:1299.
Ogbera AO, Ekpebegh C. Diabetes mellitus in Nigeria: The past, present and future. World J Diabetes 2014;5:905-11.
Michael JF. Microvascular and macrovascular complications of diabetes. Clin Diabetes 2008;26:77-82.
Townsend R. Mechanism of Diabetic Nephropathy. Renal and Urology News: 2007;1-4.
Carmines PK. The renal vascular response to diabetes. Curr Opin Nephrol Hypertens 2010;19:85-90.
Milovanceva-Popovska M, Dzikova S. Progression of diabetic nephropathy: Value of intrarenal resistive index (RI). Prilozi 2007;28:69-79.
Saif A, Soliman NA, Abdel-Hameed A. Early evaluation of renal hemodynamic alterations in type I diabetes mellitus with duplex ultrasound. Saudi J Kidney Dis Transpl 2010;21:295-9.
] [Full text]
Petersen LJ, Petersen JR, Talleruphuus U, Ladefoged SD, Mehlsen J, Jensen HA, et al.
The pulsatility index and the resistive index in renal arteries. Associations with long-term progression in chronic renal failure. Nephrol Dial Transplant 1997;12:1376-80.
Dawha S, Ayoola O, Ibitoye B, Ikem R, Arogundade F. An assessment of factors influencing resistivity and pulsatility indices in diabetes mellitus. Trop J Nephrol 2017:9;15-22.
Kasiulevivius V, Sapoka V, Filipaviviute R. Sample size calculation in epidemiological studies. Gerontologija 2006;7:225-31.
KDOQI clinical practice guidelines and clinical practice recommendations for diabetes and chronic kidney disease. Am J Kidney Dis 2007;49:S12-154.
Platt JF, Ellis JH, Rubin JM, DiPietro MA, Sedman AB. Intrarenal arterial Doppler sonography in patients with nonobstructive renal disease: Correlation of resistive index with biopsy findings. AJR Am J Roentgenol 1990;154:1223-7.
Saeed Z, Mirza W, Sayani R, Sheikh A, Yazdani I, Hussain SA. Sonographic measurement of renal dimensions in adults and its correlates. Int J Collab Res Int Med Public Health 2012;4:1626-41.
Singh GR, Hoy WE. Kidney volume, blood pressure, and albuminuria: Findings in an Australian aboriginal community. Am J Kidney Dis 2004;43:254-9.
Brkljacić B, Mrzljak V, Drinković I, Soldo D, Sabljar-Matovinović M, Hebrang A, et al.
Renal vascular resistance in diabetic nephropathy: Duplex Doppler US evaluation. Radiology 1994;192:549-54.
Ishimura E, Nishizawa Y, Kawagishi T, Okuno Y, Kogawa K, Fukumoto S, et al.
Intrarenal hemodynamic abnormalities in diabetic nephropathy measured by duplex Doppler sonography. Kidney Int 1997;51:1920-7.
Kawai T, Kamide K, Onishi M, Yamamoto-Hanasaki H, Baba Y, Hongyo K, et al.
Usefulness of the resistive index in renal Doppler ultrasonography as an indicator of vascular damage in patients with risks of atherosclerosis. Nephrol Dial Transplant 2011;26:3256-62.
Baxter GM, Sidhu PS. Ultrasound of the Urogenital System. New York, Stuttgart: Thieme; 2006. p. 286.
Mancini M, Masulli M, Liuzzi R, Mainenti PP, Ragucci M, Maurea S, et al.
Renal duplex sonographic evaluation of type 2 diabetic patients. J Ultrasound Med 2013;32:1033-40.
Koenhemsi L, Toydemir S, Ucmak M, Gonul R, Or ME. Evaluation of early renal disease in bitches with pyometra based on renal Doppler measurements. Vet Med 2016;61:344-7.
Radermacher J, Mengel M, Ellis S, Stuht S, Hiss M, Schwarz A, et al.
The renal arterial resistance index and renal allograft survival. N Engl J Med 2003;349:115-24.
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. [Full text]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]