KIDNEY TRANSPLANTATION Effect of Visceral, Subcutaneous and Retroperitoneal Adipose Tissue on Renal Function After Living Donor Nephrectomy: A Retrospective Analysis of 69 Cases Murat Ferhat Ferhatoglu1*, Eray Atli2, Alp Gurkan1 Purpose: Recent studies reported that the presence of metabolic syndrome is closely correlated with impaired kid- ney function after living donor nephrectomy. Since the measurement of body mass index cannot differentiate the amount of body adipose tissue from total body weight, body mass index is not a reliable parameter for determining metabolic syndrome. In the present study, we investigated the correlation between body adipose tissue and kidney function recovery following living donor nephrectomy. Materials and Methods: The patients who underwent living kidney donor nephrectomy consequently from July 2016 through December 2017 were enrolled in the study. We preoperatively measured the visceral (VAdT), ret- roperitoneal (RPAdT), and subcutaneous (SCAdT) adipose tissue volume by a computed tomography scan. Body mass index, adipose tissue measurements, and postoperative estimated glomerular filtration rate (eGFR) were evaluated. Results: The decrease between preoperative eGFR, and the first day, the first month and the sixth month eGFR after surgery were statistically significant (P = .001; P = .001; P = .001, respectively). The negative correlation between VAdT/SCAdT measurements and changes in eGFR at the first and the sixth postoperative month com- pared to preoperative eGFR were statistically significant (P = .049; P = .041, respectively). Additionally, RPAdT measurements and changes in eGFR at the first and the sixth postoperative month compared to preoperative eGFR (decreasing as RPAdT value increased) were statistically significant (P = .035; P = .026, respectively). Conclusion: According to a preoperative computed tomography scan, VAdT, RPAdT, and VAdT-to-SAdT ratio can predict impaired kidney function recovery. Furthermore, RPAdT measurement is a new variable to predict the impaired kidney function after living donor nephrectomy. Keywords: adipose tissue; donor nephrectomy; kidney; metabolic syndrome; retroperitoneal; visceral INTRODUCTION Being a kidney donor increases the risk of renal impairment and the possibility of being a chronic kidney disease patient in the future.(1,2) Recent studies showed that the presence of metabolic syndrome is an independent risk factor for the development of chronic kidney disease.(1,3-6) Metabolic syndrome has two main components, increased body mass index (BMI) (obesi- ty) and increased blood pressure (hypertension). We think the selection of a living kidney donor is a crucial process. Many studies or guidelines have tried to present the best criteria for the selection of the liv- ing kidney donors.(7-9) However, none of these studies or guidelines may fully guarantee the safety of the liv- ing donor in perioperative or postoperative period. The calculation of BMI gives no idea about the distribution of abdominal adipose tissue or visceral obesity, which have been linked to the risk of microalbuminuria and chronic kidney disease.(1,3,10,11) For this reason, the cur- rent living donor selection criteria should be modified. In the present study, we aimed to assess the distribu- tion of abdominal adipose tissue and recovery of kid- 1Department of General Surgery, Istanbul Okan University, Faculty of Medicine, Tuzla Istanbul 34759, Turkey. 2Department of Radiodiagnostics, Istanbul Okan University, Faculty of Medicine, Tuzla Istanbul 34759, Turkey. *Correspondence: Department of General Surgery, Istanbul Okan University, Faculty of Medicine, Tuzla Istanbul 34959, Turkey Tel: +905553214793, Fax: +902164449863, E-mail: ferhatferhatoglu@yahoo.co.uk Received September 2019 & Accepted December 2019 ney function after living kidney donor nephrectomy. Also, this study may show the importance of preoper- ative evaluation of adipose tissue potentially may lead to getting better outcomes in living donors after donor nephrectomy procedure. MATERIALS AND METHODS Selection of donor candidates All of the kidney donor candidates had detailed blood and urine tests and renal computed tomography (CT) angiography. Candidates who were found to be healthy were considered as kidney donors. Patients with comor- bid disease and alcohol and cigarette dependence were not considered as living kidney donor candidates in the institution where the present study was conducted. Inclusion criteria: The patients who underwent living kidney donor nephrectomy consequently from July 2016 through December 2017 at Istanbul Okan Univer- sity Hospital and Research Center were enrolled in this observational cohort study. Exclusion criteria: The patients who had computed to- mography angiography at another institution, who did Urology Journal/Vol 17 No. 4/ July-August 2020/ pp. 379-385. [DOI: 10.22037/uj.v0i0.5558 ] not want to participate in the study protocol, and who had a follow-up period of less than six months were ex- cluded from the study (Figure 1). Surgical procedure The same two surgeons performed all surgical proce- dures by using the video-assisted mini-incision tech- nique, which was described and standardized by Choi KH et al.(12) Evaluation of the individuals: We evaluated routine blood tests, renal CT angiography for all individuals. After laparoscopic kidney donor nephrectomy, rou- tine blood tests were performed until the patients were discharged. Since Choi et al. stated that the time when the renal functions were stabilized in kidney donor pa- tients was six months after surgery, we followed our patients for six-months.(13) We calculated their estimat- ed glomerular filtration rate (GRF) (calculated by using Modification of Diet in Renal Disease Formula, GFR (mL/min/1.73 m2) = 175 × (Scr)-1.154 × (Age)-0.203 × (0.742 if female) × (1.212 if African American))(14) pre- operatively, first, and the sixth month of the nephrec- tomy. Body mass index (BMI) was calculated accord- ing to the formula: the bodyweight/ height in meters squared. Patients with BMI ≥ 30kg/m2 were defined as obese.(15) The body surface area was calculated accord- ing to the formula described by Mosteller.(16) Radiologic evaluation Total intraabdominal and subcutaneous (SCAdT) adi- pose tissue were measured at the level of the umbilicus using CT axial slice (Optima CT 660, General Electric Medical Systems, Milwaukee, Wisconsin, USA) (Fig- ure 2). Total intraabdominal adipose tissue was divided into two part including retroperitoneal adipose tissue (RPAdT) and visceral adipose tissue (VAdT) (Total intraabdominal adipose tissue= VAdT + RPAdT). Af- ter the margin of the intraabdominal cavity and sub- cutaneous soft tissue were delineated on the CT slice, the volumes of total intraabdominal and SCAdT were calculated by a single radiologist (10-year experienced) using CT software (GE AW 4.7 Work Station, Volume and Threshold tools, General Electric Medical Systems, Milwaukee, Wisconsin, USA). This software electroni- cally defines adipose tissue volume by setting the atten- uation values for a region of interest within a range of -50 to -250 Hounsfield. RPAdT was calculated in the same way margining border of the retroperitoneal area. The VAdT was calculated by subtracting the RPAdT value from total intraabdominal adipose tissue. Ethical approval: All procedures performed in studies involving human participants were following the Hel- sinki declaration and its later amendments or compa- rable ethical standards. The study protocol was also reviewed and approved by the ethics committee of Is- tanbul Okan University, Istanbul (No: 104, Date: March 13, 2019). All individuals gave written informed con- sent Statistical analysis NCSS (Number Cruncher Statistical System) 2007 (Kaysville, Utah, USA) was used for statistical anal- ysis. Descriptive statistical methods (mean, standard deviation, median, frequency, percentage, minimum, maximum) were used to evaluate the study data. The suitability of the quantitative data for normal distribu- tion was tested with the Shapiro-Wilk test and graphical analysis. The Kruskal-Wallis test was used for compar- ison of more than two groups of quantitative variables those were not normally distributed. Bonferroni cor- rected paired evaluations were used for intra-group comparisons of quantitative variables showing normal distribution, repeated measures analysis of variance, and paired comparisons. Wilcoxon signed-ranks test was used for intra-group comparisons of quantitative variables that were not normally distributed. Spearman correlation analysis was used to evaluate the relation- ships between quantitative variables (Table 1).(17) Sta- tistical significance was accepted as p < .05. RESULTS Twenty-seven caucasian male, thirty-two caucasian Kidney Transplantation 380 Table 1. Spearman Correlation coefficient interpretation guideline r Description of strength 0.00 — 0.19 Very weak 0.20 — 0.39 Weak 0.40 — 0.59 Moderate 0.60 — 0.79 Strong 0.80 — 1.00 Very strong Table 2. Patients characteristics and adipose volume measurements Age (year) Min-Max (Median) 20-71 (44) Mean ± SD 44.09 ± 13.54 Gender Female 32 (54.2%) Male 27 (45.8%) BMI (kg/m2) Min-Max (Median) 18.6-40.23 (28.2) Mean ± SD 28.30 ± 4.44 BSA (m2) Min-Max (Median) 1.33-2.28 (1.85) Mean ± SD 1.86±0.19 Hospitalization time (day) Min-Max (Median) 2-9 (3) Mean ± SD 3.61 ± 1.39 SCAdT (cm3) Min-Max (Median) 4.58-190.03 (35.98) Mean ± SD 54.13 ± 47.42 VAdT (cm3) Min-Max (Median) 376.89-10368.71 (2923.85) Mean ± SD 2846.84 ± 1694.85 RPAdT (cm3) Min-Max (Median) 39.49-4690.36 (1028.25) Mean ± SD 1200.21 ± 879.44 VAdT/SCAdT Min-Max (Median) 5.79-312.77 (71.41) Mean ± SD 84.99 ± 70.13 *BMI: Body mass index, BSA: Body surface area, SCAdT: Subcutaneous adipose tissue, VAdT: Visceral adipose tissue, RPAdT: Retro- peritoneal adipose tissue, PAdT: Peritoneal adipose tissue Effect of adipose tissue on kidney function after donor nephrectomy- Ferhatoglu et al. female, included to study with a mean age was 44.09 ± 13.54, and follow-up time was six-months. Table 2 shows patient characteristics and adipose volume meas- urements. The relationship between preoperative eGFR and the first day, first month and sixth month eGFR decrement (23.07 ± 23.2 mL/min/m2, 36.67 ± 14.69 mL/min/m2, 31.71 ± 13.66 mL/min/m2) were statistically significant (p = .001; p = .001; p = .001, respectively; Bonferroni Test, p <.01) (Figure 3). BMI, VAdT and SCAdT measurements had a statisti- cally significant correlation with each other (p = .035, Pearson correlation, p <.05). Relationship between changes in eGFR and adipose tissue measurements was demonstrated on Table 3. The negative correlation between VAdT/SCAdT measurements and changes in eGFR at the first and the sixth postoperative month compared to preoperative eGFR (decreasing as VAdT/ SCAdT value increased) were statistically significant (r = -0.256; p = .049 and r = -0.267; p = .041, respective- ly). Additionally, RPAdT measurements and changes in eGFR at the first and the sixth postoperative month compared to preoperative eGFR (eGFR decreases as RPAdT value increase) were statistically significant (r = -0.232; p = .035 and r = -0.205; p = .026, respective- ly). Also, there is a positive correlation between chang- es in eGRF at the sixth postoperative month in patients with BMI ≥ 30 kg/m2 (r = 0.275; p = .035). However, no correlation was observed between eGFR changes and BMI in patients with BMI < 30 kg/m2. DISCUSSION We investigated the accuracy of evaluating the fat com- position of the kidney donor to predict delayed kidney function, and find out that RPAdT, VAdT, and VAdT- to-SCAdT ratio are significantly associated with an im- paired kidney function of the donor patient. It is well known that metabolic syndrome and its com- ponents, obesity, hyperglycemia, and hypertriglyc- eridemia are closely correlated with impaired kidney function.(18,19) Also, many studies demonstrated that the presence of obesity is linked to impaired postoperative kidney function in kidney donors.(1,3,18,19) Studies from the USA and Sweeden (The Framingham Offspring Effect of adipose tissue on kidney function after donor nephrectomy- Ferhatoglu et al. Table 3. Evaluation of the Relationship Between Changes in eGFR and BMI and Adipose Tissue Preoperative-1st day Preoperative-1st Month Preoperative-6th month Donor BMI (kg/m2) ≥ 30 (Obese) (n=29) r 0.023 0.038 -0.275 p .860 -775 .035* <30 (Non-obese) (n=40) r 0.157 0.023 0.038 p .235 .860 .775 SCAdT r 0.267 0.034 0.189 p .041* .797 .152 VAdT r 0.097 -0.301 -0.428 p .465 .021* .036* RPAdT r 0.122 -0.232 -0.205 p .359 .035* .026* VAdT/SCAdT r -0.099 -0.256 -0.467 p .457 .049* .041* d r = Spearman’s correlation coefficient *p < 0.05 **p < 0.01 eGFR: Estimated glomerular filtration rate. BMI: Body mass index. SCAdT: Subcutaneous adipose tissue. VAdT: Visceral adipose tissue. RPAdT: Retroperitoneal adipose tissue. Figure 1. Scheme of the present study Vol 17 No 04 July-August 2020 381 cohort and the Hypertension Detection and Follow-up Program) have revealed that higher BMI is linked with impaired kidney function.(20-22) Locke et al. also showed that obesity was independently associated with an in- creased risk for ESRD in living kidney donors.(23) BMI can be easily calculated, and it has been generally used as a reliable anthropometric index of obesity.(24) However, BMI is not a reliable anthropometric meas- ure due to changes in body fluid distribution in patients candidate for kidney transplantation. Moreover, gener- ally accepted BMI norms for determining obesity do not reflect the degree of visceral obesity.(25,26) Addition- ally, whether visceral obesity quantitatively measured by VAdT, SCAdT, RPAdT, and VAdT-to-SCAdT quo- tient before the surgery estimate results in living kidney donor have not been well researched. Numerous studies prove that VAdT has various endo- crine, metabolic, and inflammatory roles.(27-30) Many hypotheses have been proposed to explain this enigma of VAdT and metabolic syndrome. The bloodstream of peritoneal and retroperitoneal fatty tissue differs from each other. One idea is that the veins of peritoneal fatty tissue drain into the portal venous system. This drainage may cause an increase in free fatty acid levels in the liv- er, which may lead to insulin resistance, high triglycer- ide concentrations, and low HDL cholesterol concentra- tions.(31,32) Also, Naya et al. demonstrated the increased proinflammatory effect of visceral fat accumulation.(26) Cornier MA et al. showed the role of elevated free fat- ty acid levels in the portal system, and the endocrine role of adipokines in metabolic syndrome.(33) We think, VAdT analysis (r = -0.428; p = .036, moderate correla- tion at sixth month eGFR change, Spearman correlation analysis) might be a more reliable and precise parame- ter to predict a metabolic syndrome component and the possibility of incoming chronic kidney disease follow- ing donor nephrectomy than BMI (r = -0.275; p = .035; weak correlation at sixth month eGFR change, Spear- Kidney Transplantation 382 Figure 2. A. Demonstration of SCAdT, VAdT, RPAdT*; B. VAdT; C. RPAdT; D. SCAdT *SCAdT: subcutaneous adipose tissue, VAdT: Visceral adipose tissue, RPAdT: Retroperitoneal adipose tissue Figure 3. Estimated glomerular filtration rate in preoperative and postoperative period (calculated by using Modification of Diet in Renal Disease Formula, GFR (mL/min/1.73 m2) = 175 × (Scr)-1.154 × (Age)-0.203 × (0.742 if female) × (1.212 if African American)); PO D: Postoperative Day, PO M: Postoperative Month Effect of adipose tissue on kidney function after donor nephrectomy- Ferhatoglu et al. man correlation analysis), which is affected by different determinants, including adipose tissue, muscles, bones, body water, and other organs. Lee et al. showed the importance of visceral and subcu- taneous adipose tissue in estimating forthcoming kid- ney disease in kidney donors.(1) Like the study of Lee et al., we found a negative correlation between eGFR and VAdT/SCAdT ratio (r = -0.467; p = .041; moderate cor- relation at sixth-month eGFR change, Spearman corre- lation analysis). Previous studies proved that the VAdT- to-SCAdT ratio is an indicator of visceral obesity.(34) Several studies demonstrated negative outcomes of ele- vated VAdT-to-SCAdT ratio.(1,3,35,36) Ghigliotti et al. showed the different cytokine synthesis profile of VAdT and SCAdT, and proposed that, although the VAdT has more tendency to produce proinflammatory cytokines such as TNF- and IL-6, SCAdT has more tendency to produce anti-inflammatory cytokines.(37) We think defining the imbalance between visceral and subcutaneous adipose tissue and the probability of ex- cessive inflammation, which is a known factor for im- paired kidney functions, may ease to estimate fort com- ing delayed kidney function of the donor patient. Retroperitoneal fat is similar to peritoneal fat, which is associated with metabolic syndrome, and related to inflammation, hypertension, and obesity.(26) Another interesting finding of our study demonstrated that the amount of RPAdT was correlated with the decrease in eGFR after donor nephrectomy (r = -0,205; p = .026, the weak correlation at sixth-month eGFR change, Spear- man correlation analysis). Unlike the visceral venous system, the venous system of the retroperitoneal fatty tissue drains into kidney veins or caval venous systems, which leads to a "fatty kidney" which is associated with hypertension. Also, this adipose tissue consists of an increased amount of brown adipose tissue, which has a known interaction with obesity and metabolic syndrome ergo possible cause of delayed kidney function.(38) Even it has impressive outcomes, this study should be considered in light of several limitations. First, retro- spective, single-institution conducted nature, and the limited number of individuals are the main limitations of the present study. Second, the possibility of sam- pling bias exists in terms of patient inclusion in the study group, because six patients (6%) were excluded from the study protocol, only because they had not un- dergone preoperative radiological evaluation at anoth- er institution. Therefore, there was likely to selection bias in the study. We think performing this research in the prospective form with longer follow-up time would improve the reliability and quality of the study. More- over, overlooking the comorbidities may be the third limitation of the present study. However, living kidney donors are not drawn from the general population, and they are healthy at baseline. Also, living donors are very carefully screened in preoperative evaluation, and the impact of obesity might be different in these health- ier individuals. 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