The renal compartment: a hydraulic view
© Cruces et al.; licensee Springer. 2014
Received: 9 August 2014
Accepted: 27 September 2014
Published: 23 October 2014
The hydraulic behavior of the renal compartment is poorly understood. In particular, the role of the renal capsule on the intrarenal pressure has not been thoroughly addressed to date. We hypothesized that pressure and volume in the renal compartment are not linearly related, similar to other body compartments.
The pressure-volume curve of the renal compartment was obtained by injecting fluid into the renal pelvis and recording the rise in intrarenal pressure in six anesthetized and mechanically ventilated piglets, using a catheter Camino 4B® inserted into the renal parenchyma.
In healthy kidneys, pressure has a highly nonlinear dependence on the injected volume, as revealed by an exponential fit to the data (R2 = 0.92). On the contrary, a linear relation between pressure and volume is observed in decapsulated kidneys. We propose a biomechanical model for the renal capsule that is able to explain the nonlinear pressure-volume dependence for moderate volume increases.
We have presented experimental evidence and a theoretical model that supports the existence of a renal compartment. The mechanical role of the renal capsule investigated in this work may have important implications in elucidating the role of decompressive capsulotomy in reducing the intrarenal pressure in acutely injured kidneys.
KeywordsCompartment syndrome Renal capsule Intrarenal pressure Kidney biomechanics
Compartment syndrome is the final result of a process that begins with the persistent increase in pressure within a tissue or parenchyma to such an extent that it is capable of altering the regional vascular inflow. Compartment syndrome may culminate in local organ failure, and if the damage persists, multiple organ failure may occur, resulting in the death of the patient. This is true for any body compartment surrounded by a rigid or semi-rigid structure, a situation often found in intracranial hypertension syndrome or abdominal compartment syndrome ,. From a hydraulic point of view, the ‘renal compartment’, whose content and structure are the parenchyma and renal capsule, respectively, should not be different from other body compartments.
In analogy to the intracranial hypertension syndrome, a sudden increase in fluid volume inside the renal parenchyma can result in a substantial intrarenal pressure and, as a consequence, a decrease in the renal perfusion pressure . In effect, acutely injured kidneys where edema is present typically involve ischemic regions of the outer medulla due to a reduction in the vascular inflow ,. From a clinical perspective, the venous congestion due to an increase of the vascular permeability to proteins, as well as the decrease of the intrarenal perfusion pressure increase the risk of developing a new or persistent septic acute kidney injury (AKI) .
The present study aims to understand, both from experimental and biomechanical approaches, the functional dependence between the renal compartment volume increments and changes in the intrarenal pressure mediated by the renal capsule. We hypothesize that pressure and volume in the renal compartment are not linearly related, and may present a functional dependence similar to those found in other compartmental syndromes.
2.1 Animal preparation
This study used anesthetized domestic large white piglets purchased from a local vivarium specialized in this species. The Universidad Andrés Bello Ethics Committee approved the experimental protocol. All experimental procedures were in accordance with the Guiding Principles in the Care and Use of Laboratory Animals adopted by the American Physiological Society. The study was powered to detect an increase in intrarenal pressure. Sample size needed to achieve an 80% study power was six, with a 0.05 one-sided significance level and a standard deviation of 33% .
2.1.1 Surgical preparation and anesthesia
Animals were premedicated with intramuscular midazolam (0.5 mg/kg), methadone (0.5 mg/kg), and ketamine (15 mg/kg), followed by induction with intravenous propofol (3 mg/kg). Tracheal intubation was performed with a cuffed tracheal tube (5.0-mm internal diameter; Mallinckrodt Shiley, St. Louis, MO, USA) for inhalation anesthesia with isoflurane 1.5%. An adequate level of anesthesia is assumed if reflexes are absent. Anesthesia and neuromuscular blockade were maintained by continuous infusion of propofol (10 mg/kg/h), fentanyl (5 μg/kg/h), and vecuronium (0.3 mg/kg/h) throughout the all experiments which lasted for less than 1 h. Heart rate, mean arterial pressure, and temperature were continuously monitored during the whole duration of the experiment. Before laparotomy, PaO2, pH, PaCO2, serum creatinine, and hemoglobin were assessed with an i-STAT® (Abbott Laboratories, Princeton, NJ, USA) in blood samples from the arterial catheter.
2.1.2 Mechanical ventilation
Animals were ventilated with anesthesia workstation Fabius GS® premium (Dräger Medical, Lübeck, Germany) using the volume control mode. Initial settings were: V T = 10 mL/kg, PEEP = 5 cmH2O, fraction of inspired oxygen = 0.4, inspiratory time = 1.0 s, and respiratory rate (RR) = 20 breaths/min. RR was adjusted to achieve a partial pressure of carbon dioxide (PaCO2) 40 ± 10 Torr.
2.1.3 Pressure-volume curve protocol
While under anesthesia, the animals were euthanized by 10% potassium chloride infusion until the detection of ventricular fibrillation or asystole.
2.2 Statistical analysis
Data are expressed as mean values ± SEM. Normality was assessed with the Anderson-Darling test. The Wilcoxon signed-rank test and the Friedman test with Bonferroni correction were conducted to compare consecutive measurements of studied variables. Significance was set at P < 0.05. All statistical analyses were performed using SPSS 20.0 (SPSS Inc., Chicago, IL, USA).
Baseline characteristics of the piglets included in the study
97 ± 11
85.5 ± 5.7
37.6 ± 0.2
7.43 ± 0.03
171.2 ± 6.2
43.1 ± 3.1
Serum creatinine (mg/dL)
1.13 ± 0.05
9.0 ± 0.3
Pressure-volume data in the renal compartment
Intrarenal pressure (Torr)
12.0 ± 2.1
17.5 ± 2.9
20.2 ± 3.4
31.2 ± 6.8
70.8 ± 16.7
where p is the intrarenal pressure and ΔV is the volume of the normal saline injected to the renal pelvis.
3.1 Biomechanical model
In AKI, a frequent finding is the increase in the kidney volume due to edema . Further, hypoperfusion of the outer medulla is common in many forms of AKI -. In view of our results, hypoperfusion may be explained by a reduction of the renal perfusion pressure ostensibly caused by the increase of intrarenal pressure due to the volume increment. This idea is supported by the fact that the use of vasodilators to revert renal hypoperfusion has been ineffective to restore blood flow -, indicating that renal perfusion is not controlled by vasomotor tone but rather by renal parenchymal pressure. Concordantly, recent studies in an ischemia-reperfusion murine model demonstrate that preventing the rise in intrarenal pressure caused by interstitial edema by making a small incision in renal capsule attenuates the risk of functional renal impairment. These findings suggest that a rise in parenchymal pressure may be contributed to the acute kidney injury caused by ischemic insult .
We have studied the dependence of the intrarenal pressure on the fluid volume in the porcine intact kidney. A highly nonlinear relation between the intrarenal pressure and the injected volume was found, which confirms the existence of a mechanical behavior commonly observed in organs confined by a rigid or semi-rigid continent, which we refer to here as the renal compartment. In contrast, decapsulted kidneys present a pressure-volume linear relation, thus confirming the role of the renal capsule as a continent. From a biomechanical analysis, it can be concluded that the observed nonlinear pressure-volume relation cannot be solely explained by the confinement conferred by the renal capsule, suggesting that above a certain level of intrarenal pressure, tissue recruitment at the kidney periphery occurs in order to sustain higher levels of intrarenal pressure. The mechanical role of the renal capsule investigated in this work may have important implications in elucidating the role of decompressive capsulotomy in preventing the rapid intrarenal pressure increase in acutely injured kidneys (e.g., kidney transplantation). Future studies could assess the effect of renal decapsulation on renal blood flow, renal oxygenation and perfusion, microcirculation, and renal function in acutely injured kidneys.
acute kidney injury
partial pressure of carbon dioxide
partial pressure of oxygen
The authors wish to thank Dr. Felipe Cavagnaro (Chairman of Pediatric Nephrology, Clínica Alemana de Santiago, Chile) and Dr. Francisco Cano (Chairman of Pediatric Nephrology, Hospital Luis Calvo Mackena, Chile) for their feedback and comments in the preparation of this manuscript. This work was supported by grants SOCHIPE 2012001 (PC), FIAC UAB 1102 (PL and FL), and Fondecyt 11121224 (DH).
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