Renal Compression in Heart Failure: The Renal Tamponade Hypothesis

State-of-the-Art Review

Eva M. Boorsma, MD; Jozine M. ter Maaten, MD, PHD; Adriaan A. Voors, MD, PHD; Dirk J. van Veldhuisen, MD, PHD

JACC Heart Fail. 2022;10(3):175-183.

Abstract and Introduction

Abstract

Renal dysfunction is one of the strongest predictors of outcome in heart failure. Several studies have revealed that both reduced perfusion and increased congestion (and central venous pressure) contribute to worsening renal function in heart failure. This paper proposes a novel factor in the link between cardiac and renal dysfunction: "renal tamponade" or compression of renal structures caused by the limited space for expansion. This space can be limited either by the rigid renal capsule that encloses the renal interstitial tissue or by the layer of fat around the kidneys or by the peritoneal space exerting pressure on the retroperitoneal kidneys. Renal decapsulation in animal models of heart failure and acute renal ischemia has been shown effective in alleviating pressure-related injury within the kidney itself, thus supporting this concept and making it a potentially interesting novel treatment in heart failure.

Introduction

The kidney plays a central role in heart failure (HF), and several large studies have shown that renal dysfunction is one of the most powerful predictors of outcome in HF.^[1,2] Already in 1990 it was demonstrated that the kidney is very sensitive to changes in perfusion. When cardiac index decreases by 25%, renal blood flow decreases by as much as 50%.^[3] Later, several groups showed that reduced renal perfusion is among the strongest determinants of glomerular filtration rate (GFR) in HF.^[4–6] Further studies in this field revealed that not only reduced renal perfusion but also, importantly, increased central venous pressure contribute to a decrease in renal function.^[7,8] Ever since, several studies have investigated the associations between clinical factors and renal congestion. Yet, the area of cardiorenal interplay remains complex.

In the present paper, we discuss the 3 mechanisms that, individually or combined, may lead to renal congestion as a result of intrarenal or extrarenal compression. Another (classic) example of renal injury as a result of compression can be found in the Page kidney: a clinical syndrome of diminished renal function and/or hypertension as a result of external compression on the kidney, most commonly subcapsular hematoma.^[9] The fact that the kidney is surrounded by a rigid and nonexpandable capsule plays a crucial role in the Page kidney and in renal compression in HF.^[10,11] We will discuss these mechanisms and will coin a novel term for this: the "renal tamponade" hypothesis.

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Table 1. Historical Findings Indicating Pressure-Related Damage to the Kidney
Increased intracapsular pressure
Preclinical studies ^a	Type of Animal (N)	Type of Intervention	Outcome(s)
Wegria et al (1955)^46b	Mongrel dogs	Clamping of the renal vein	• Proteinuria after renal venous pressure >250 mm H₂O
Stone and Fulenwider (1977)⁴⁷	Monkeys (12)	Renal ischemia induced by clamping of the suprarenal aorta, unilateral renal decapsulation	• Preservation of creatinine and urea clearance in the decapsulated kidney
Burnett and Knox (1980)¹⁷	Mongrel dogs (10)	Clamping of the renal vein	• Increased renal interstitial pressure • Decreased FeNa during volume expansion
Khraibi et al (1977)⁴⁸	Wistar rats (19)	Renal ischemia induced by clamping of the suprarenal aorta, unilateral renal decapsulation, acute volume expansion	• Attenuation of renal interstitial pressures after volume expansion in decapsulated kidney
García-Estañ and Roman (1990)⁴⁹	Sprague-Dawley rats (27)	Renal decapsulation and infusion of ANP	• Increase in interstitial medullary pressure after ANP infusion • Normalization of cortical interstitial pressure after ANP infusion and decapsulation
Komuro et al (2017)¹⁸	Wistar rats (9)	Saline administration until CVPs of 10 and 15 mm Hg were attained	• Correlation between CVP and renal interstitial pressure (r = 0.95) • Reduced medullary perfusion, as assessed with contrast-enhanced ultrasonography
Shimada et al (2018)²⁰	Sprague-Dawley rats (10)	Clamping of the renal vein, renal decapsulation	• Increased renal interstitial pressure • Proteinuria • Increased expression of markers of tubular damage • Decreased GFR and urine production • Attenuation of the above after decapsulation
Cruces et al (2018)⁴⁴	Piglets (18)	Ischemia-reperfusion with or without renal decapsulation versus sham procedure	• Lower intrarenal pressure after renal decapsulation, as compared with ischemia without decapsulation and/or sham procedure • Lower renal lactate release after renal decapsulation, as compared with ischemia without decapsulation and/or sham procedure
Clinical studies	Study Population (N)	Type of Intervention	Outcome(s)
Stone and Fulenwider (1977)⁴⁷	Hemorrhagic shock patients with acute tubular necrosis (21)	Unilateral renal capsular incision	• Greater renal plasma flow on the decapsulated side • Greater urine flow on the decapsulated side • Reduced incidence of anuria/oliguria as compared with anticipated incidence (7% vs 75%)
Nijst et al (2017)²³	• Euvolemic HFrEF (40) • Euvolemic HFpEF (40)	• Infusion of 1 L hydroxyethyl starch 6% • Intravenous bolus of loop diuretic	• Blunting of intrarenal venous flow patterns after volume expansion • Return to baseline after loop diuretic administration
De la Espriella-Juan et al⁵⁰	Acute HF (1)	Aggressive decongestive treatment	• Normalization of renal venous flow patterns
Ter Maaten et al (2021)²²	Acute HF (15)	Standard of care decongestive treatment	• Normalization of renal venous flow patterns
Increased perirenal pressure
Preclinical studies	Type of Animal (N)	Type of Intervention	Outcome(s)
Hou et al (2014)⁵¹	Wistar rats (10)	High-fat versus normal diet	• PRAT was associated with infrarenal aortic endothelial dysfunction • PRAT was associated with albuminuria in obese rats
Ma et al (2016)³⁰	Pigs (14)	High-fat/high-fructose versus standard diet	• PRAT in obese pigs with larger PRAT vasodilation of the renal artery was impaired. This was restored after TNF-α blockage.
Cops et al (2020)⁵²	Sprague-Dawley rats (16)	• Surgical wire constriction on IVC • Randomization to sedentary versus moderately intense endurance exercise	• Endurance exercise lowered perirenal fat pad/tibia length ratio, whereas body weight remained similar to that of sedentary rats • Abdominal pressure was lowered in the endurance group • Cystatine C was lower in the endurance group • No differences between other indices of kidney function could be found
Clinical studies	Study Population (N)	Type of Intervention/Observation	Outcome(s)
Lamacchia et al (2011)⁵³	Type 2 diabetes (151)	Quantification of peri- and pararenal fat thickness on ultrasound	• PRAT was independently associated with eGFR (β = −0.327) after correction for WC and BMI.
Sun et al (2013)⁵⁴	• Obese healthy volunteers (67) • Age- and sex-matched healthy lean volunteers (34)	Quantification of peri- and pararenal fat thickness on ultrasound	• PRAT was higher in obese patients with albuminuria than in obese patients without albuminuria
Geraci et al (2018)²⁴	Hypertension (269)	Quantification of peri- and pararenal fat thickness on ultrasound	• Correlation between PRAT and eGFR (r = −0.284) • In multivariable regression, PRAT remained an independent predictor of eGFR after correction for BMI and WC
Ricci et al (2018)⁵⁵	Morbid obesity (284)	Sleeve gastrectomy	• PRAT was an independent predictor of systolic blood pressure in obese subjects (β = 0.160) after rigorous correction for known risk factors • PRAT significantly reduced after sleeve gastrectomy
D'Marco et al (2019)²⁶	Chronic kidney disease (classes I–V) (103)	Perirenal fat between renal cortex and hepatic/splenic border measurement on ultrasound	• PRAT was larger in patients with prediabetes, CKD stage 4 or 5, and higher triglyceride levels but not in those with a history of hypertension
Koo et al (2020)²⁵	Community-based cohort (3,919)	Estimation of PRAT on CT	• PRAT was associated with renal (OR 2.05) and aortic (OR 1.11) atherosclerosis
Notohamiprodjo et al (2020)⁵⁶	• Healthy normoglycemic (230) • Prediabetes (87) • Type 2 diabetes (49)	Quantification of renal sinus fat volume on CMR	• Diabetes (β = 7.34) and prediabetes (β = 7.13) were significantly associated with more renal sinus fat, compared with normoglycemia in control individuals.
Spit et al (2020)³¹	Type 2 diabetes (51)	Quantification of renal sinus fat volume on CMR	• Correlation between renal sinus fat and GFR (r = -0.38) • Correlation between renal sinus fat and effective renal plasma flow (r = −0.38)
Fang et al (2020)⁵⁷	Type 2 diabetes (171)	Ultrasound assessment of PRAT diameter	• Correlation between PRAT and eGFR diameter (r = −0.181)
Increased intra-abdominal pressure^a
Preclinical studies	Type of Animal (N)	Type of Intervention	Outcome(s)
Harman et al (1982)⁵⁸	Mongrel dogs (7)	Insertion of inflatable bags in the peritoneum	• At 20 mm Hg, GFR decreased to <25% of baseline value • At 40 mm Hg, dogs became anuric and <7% of baseline GFR remained • CO also diminished to 37%, an effect that could be attenuated by infusion of fluids
Bishara et al (2011)⁵⁹	• Sprague-Dawley rats, aortocaval fistula, compensated (86) • Sprague-Dawley rats, aortocaval fistula, decompensated (6) • Sprague-Dawley rats, aortocaval fistula, decompensated and pretreated with NOS inhibitor (6)	Pneumoperitoneum induced by injection of air through a needle	• After IAP >14 mm Hg, GFR, urinary flow, and sodium excretion decreased • This effect was most pronounced in decompensated rats • Pretreatment with NOS inhibitor exacerbated the decline in renal function
Abu-Saleh et al (2019)⁶⁰	• Sprague-Dawley rats, sham operated (23) • Sprague-Dawley rats, aortocaval fistula, compensated (8) • Sprague-Dawley rats, aortocaval fistula, decompensated (9), and pretreated with tadalafil (6) • Sprague-Dawley rats, acute myocardial infarction (7), and pretreated with tadalafil (11) • Sprague-Dawley rats, sham treated with tadalafil (6)	Pneumoperitoneum induced by injection of air through a needle	• After IAP of 10 mm Hg RPF, GFR, urinary flow and sodium excretion all diminish • This effect is most pronounced in decompensated ACF rats • This effect is ameliorated by pretreatment with tadalafil • GFR recovered after IAP normalizes in all groups • In sham and MI rats, natriuresis increases to above baseline level after IAP is normalized, in decompensated rats natriuresis remains low
Clinical studies	Study Population (N)	Type of Intervention/Observation	Outcome(s)
Sugerman et al (1998)⁶¹	Morbidly obese (15)	• Measurement of abdominal pressure using urinary catheter manometer • Roux-en-Y gastric bypass	• Significant reduction of IAP 1 y after GBS
Nguyen et al (2001)³⁶	Morbidly obese (64)	• Randomized to either open or laparoscopic gastric bypass	• IAP increased in both groups on day 1 postoperatively • IAP returned to baseline in the laparoscopic group on day 2 postoperatively • No data on long-term change in IAP
Lambert et al (2005)⁶²	Morbidly obese (45)	• Measurement of abdominal pressure using urinary catheter manometer • Roux-en-Y gastric bypass	• Obese patients have a higher IAP compared with general population • IAP correlates to number of comorbidities • IAP is not reduced by incising the peritoneum • The first 2 days post operatively IAP increases • No long-term data on IAP after GBS
Mullens et al (2008)⁶³	Acute decompensated HF refractory to treatment (9)	Paracentesis (5) or ultrafiltration (4)	• After mechanical fluid removal IAP was significantly reduced (mean reduction 5 mm Hg) • After mechanical fluid removal, renal function improved (mean serum creatinine from 3.4 ± 1.4 mg/dL to 2.4 ± 1.1 mg/dL)
McIsaac et al (2019)³⁷	Morbidly obese (471)	Gastric bypass (sleeve gastrectomy or Roux-en-Y)	• In patients with microalbuminuria, GFR increased from 109 ± 10 mL/min to 120 ± 36 mL/min 24 months after GBS • In patients with microalbuminuria, albumin-creatinine-ratio normalized 24 months after GBS • No data on IAP either pre- or postoperatively
Rubio-Gracia et al (2020)⁶⁴	Acute decompensated HF (43)	• Measurement of abdominal pressure using urinary catheter manometer • Standard of care decongestive treatment	• Higher baseline IAP was associated with poorer diuretic and natriuretic response • Higher baseline IAP was associated with higher serum creatinine • IAP >12 mm Hg after 72 h of decongestive treatment was associated with higher mortality and rehospitalization rates

^aStudies published in any language other than English, or with no available abstract, were omitted from inclusion in this table. ^bReferences as they appear in reference list.
ACF = aortocaval fistula; ANP = atrial natriuretic peptide; BMI = body mass index; CKD = chronic kidney disease; CMR = cardiac magnetic resonance; CT = computed tomography; CVP = central venous pressure; eGFR = estimated glomerular filtration rate; FeNa = fractional excretion of sodium; GBS = gastric bypass; HF = heart failure; HFpEF = heart failure with preserved ejection fraction; HFrEF = heart failure with reduced ejection fraction; IAP = intra-abdominal pressure; IVC = inferior vena cava; mm H₂O = millimeters water pressure; NOS-inhibitor = nitric oxide synthase – inhibitor; PRAT = perirenal adipose tissue; RPF = renal plasma flow; TNF-α = tumor necrosis factor-α; WC = waist circumference.

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Renal Compression in Heart Failure: The Renal Tamponade Hypothesis

State-of-the-Art Review

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