Abstract
Background:
This study was undertaken to prospectively evaluate the impact of partial portal decompression on renal haemodynamics and renal function in patients with cirrhosis and portal hypertension.
Methods:
Fifteen consecutive patients (median age 49 years) with cirrhosis underwent partial portal decompression through portacaval shunting or transjugular intrahepatic portosystemic shunting (TIPS). Cirrhosis was caused by alcohol in 47%, hepatitis C in 13%, both in 33% and autoimmune factors in 7% of patients. Child class was A in 13%, B in 20% and C in 67% of patients. The median score on the Model for End-stage Liver Disease (MELD) was 14.0 (mean 15.0 ± 7.7). Serum creatinine (SrCr) and creatinine clearance (CrCl) were determined pre-shunt, 5 days after shunting and 1 year after shunting. Colour-flow Doppler ultrasound of the renal arteries was also undertaken with calculation of the resistive index (RI) and pulsatility index (PI). Changes in the portal vein–inferior vena cava pressure gradient with shunting were determined.
Results:
With shunting, the portal vein–inferior vena cava gradients dropped significantly, with significant increases in PI in the early period after shunting. Creatinine clearance improved in the early post-shunt period. However, SrCr levels did not significantly improve. At 1 year after shunting, both CrCl and SrCr levels tended towards pre-shunt levels and the increase in PI did not persist.
Discussion:
Partial portal decompression improves mild to moderate renal dysfunction in patients with cirrhosis. Early improvements in renal function after shunting begin to disappear by 1 year after shunting.
Keywords: Renal haemodynamics, renal function, portacaval shunting
Introduction
Renal dysfunction frequently occurs in patients with cirrhosis and portal hypertension, with symptoms ranging from an inability to concentrate urine to oliguria and renal failure. Despite its frequency, the aetiology of renal dysfunction in patients with cirrhosis and portal hypertension is not fully understood. Recent evidence suggests that increased renovascular arterial tone may be an important determinant of renal dysfunction in patients with cirrhosis.1 Despite notable splanchnic arterial vasodilatation and hyperdynamic circulation, patients with cirrhosis show increased renal arterial tone, resulting in poor renal perfusion. Specifically, the increased renal arterial tone leads to the activation of the renin–angiotensin system and increased levels of angiotensin II and aldosterone, which, in turn, favour renal artery vasoconstriction and further promote renal ischaemia and fluid retention.2
Early diagnosis of mild to moderate renal impairment in patients with cirrhosis can be difficult. Conventional renal function tests, such as serum creatinine (SrCr) and blood urea nitrogen (BUN), are not sensitive indicators of early renal impairment, with elevation of SrCr occurring only after a considerable portion of renal parenchyma is functionally impaired. In addition, determination of urine electrolytes in patients with cirrhosis is generally not reliable because most of these patients are treated withdiuretics for fluid retention and ascites. A more sensitive test to determine renal function is 24-hour creatinine clearance (CrCl), although its determination is cumbersome and often not possible in an acute-care setting.
The application of non-invasive diagnostic technologies, such as colour-flow Doppler ultrasound, in the study of renal haemodynamics can document tone in the renal artery circulation. Specifically, arterial tone can be determined with calculation of the resistive index (RI) and pulsatility index (PI).3 In patients with cirrhosis, these parameters tend to be elevated relative to those in healthy individuals or in other patients with ascites unrelated to cirrhosis and portal hypertension,4 reflecting increased tone in the renal vascular circulation.
In this study, we measured changes in renal function and renal haemodynamics occurring in patients immediately after and 1 year after partial portal decompression through transjugular intrahepatic portosystemic shunt (TIPS) or small-diameter prosthetic H-graft portacaval shunt (HGPCS) because of bleeding varices and portal hypertension. The purpose of this study was to determine if and how partial portal decompression influences renal function and haemodynamics. Our hypothesis in undertaking this study was that partial portal decompression would improve renal function by increasing renal perfusion, as determined by calculation of the RI and PI.
Materials and methods
With Institutional Review Board approval, a randomized trial comparing TIPS with small-diameter prosthetic HGPCS began in 1993.5,6 Patients with bleeding oesophagogastric or intestinal varices or bleeding from portal gastropathy secondary to cirrhosis and portal hypertension were enrolled. All patients had failed or were not amenable to endoscopic sclerotherapy or banding. Patients were randomized in pairs to TIPS or small-diameter prosthetic HGPCS through computer-generated random numbers. Shunting was always undertaken as a definitive therapy and never as a bridge to transplantation.
Prior to shunting, all patients underwent routine measurements of serum electrolytes, creatinine, BUN, albumin, SGPT (serum glutamic pyruvic transaminase) and SGOT (serum glutamic oxaloacetic transaminase), bilirubin, prothrombin time (PT), international normalized ratio (INR) and partial thromboplastin time (PTT). Ascites was defined as absent, controlled (required salt and volume restriction, as well as diuretics) or refractory (present despite full medical therapy). Encephalopathy was defined as absent, mild (encephalopathy effectively avoided/treated by lactulose and a protein-restricted diet) or severe (patient requiring hospitalization for encephalopathy despite full medical therapy). Each patient was assigned a Child class. A Model for End-stage Liver Disease (MELD) score7 was also calculated for each patient pre-TIPS or portacaval shunt.
The techniques for the construction of the small-diameter prosthetic shunt and TIPS have been described previously.5 Briefly, the small-diameter prosthetic portacaval shunt was constructed using an 8-mm, ring-reinforced polyfluorotetraethylene (PFTE) graft, measuring 3 cm from toe to toe, with bevels at 90 degrees to one another. TIPS was undertaken through cannulation of the right internal jugular vein. A Wallstent 8–10 mm in diameter bridged the right hepatic vein to the right branch of the portal vein. The stent was dilated to achieve adequate portal decompression. With each shunt, pre- and post-shunt portal vein pressures and portal vein–inferior vena cava pressure gradients were determined. Five days after shunting, shunt patency and function were assessed utilizing trans-shunt venography to measure trans-shunt pressures. Five days after shunting, all patients were haemodynamically stable, regardless of the shunt undertaken.
Fifteen consecutive patients, a subgroup of a large, randomized trial,5,6 underwent pre-shunt, post-shunt and late (1 year after shunting) assessment of renal function, including measurement of 24-hour urinary CrCl. Similarly, the RI and PI of the main renal arteries and of two intraparenchymal branches of the renal arteries were calculated before, 5 days after and 1 year after shunting using colour-flow Doppler ultrasound. Waveforms were measured at three different sites for each renal artery and at two different intraparenchymal branches of each renal artery. Colour-flow Doppler ultrasound was undertaken utilizing a 128 XP scanner with a 3.5 MHz and 2.5 MHz transducer (Acuson Corp., Mountain View, CA, USA).
The RI was calculated with electronic callipers, using the following formula:
 |
The PI was similarly calculated, using the formula:
 |
Data were compiled into a Microsoft excelspreadsheet and are presented as mean ± standard deviation (SD). Comparisons of renal function and renal haemodynamics before and after partial portal decompression were made utilizing anova matched-samples test. Comparison between patients undergoing TIPS vs. H-graft shunts were made using one-way anova or Mann–Whitney U-test. Statistical significance was accepted with 95% confidence.
Results
Beginning in 1993, 132 patients were enrolled in a prospective randomized trial comparing TIPS with small-diameter prosthetic HGPCS.5,6 Among these, 15 consecutive patients (six undergoing TIPS and nine undergoing H-graft shunts) underwent measurements of renal function and renal haemodynamics before and after shunting and at 1 year after shunting (Table 1). Their median age was 49 years. Cirrhosis was caused exclusively by alcohol in seven (47%) patients and Child classification was C in 10 (67%) patients. The median MELD score was 14.0 (mean 15.0 ± 7.7). Shunting was undertaken with urgency in 20% of patients as they experienced significant variceal recurrent bleeding after their operative evaluation. Preoperative ascites was determined to be mild in six (40%) patients (Table 1).
Table 1.
Clinical data for 15 patients undergoing partial portal decompression
| Median age, years | 49 |
|---|---|
| Gender | |
| Male | 80% |
| Aetiology of cirrhosis | |
| EtOH | 47% |
| Hepatitis C | 13% |
| EtOH + hepatitis C | 33% |
| Autoimmune causes | 7% |
| Child class | |
| A | 13% |
| B | 20% |
| C | 67% |
| MELD score | |
| Median | 14 |
| Mean ± SD | 15 ± 7.7 |
| Type of varices | |
| Oesophageal varices | 33% |
| Gastric varices | 27% |
| Oesophageal + gastric varices | 33% |
| Intestinal varices | 7% |
| Pre-shunt therapy | |
| Sclerotherapy | 65% |
| Banding | 55% |
| Circumstances of shunting | |
| Elective | 80% |
| Urgent | 20% |
| Pre-shunt ascites | |
| Controlled | 40% |
| Refractory | 20% |
| Pre-shunt encephalopathy (mild) | 20% |
EtOH, ethyl alcohol; MELD, Model for End-stage Liver Disease; SD, standard deviation
MELD score, Child class, Child–Pugh score, cause of cirrhosis, age and gender were similar in both the TIPS and HGPCS groups. Both HGPCS and TIPS always produced decreased portal pressures and portal vein–inferior vena cava pressure gradients (Table 2). There were no significant differences in pre- or post-shunt portal vein pressures or in portal vein–inferior vena cava pressure gradients between patients undergoing HGPCS or TIPS. All shunts were patent with late follow-up by colour-flow Doppler ultrasound and transvenous study.
Table 2.
Portal vein (PV) and inferior vena cava (IVC) haemodynamics before and after transjugular intrahepatic portosystemic shunt, and before and after 8-mm H-graft portacaval shunt
| Pre-shunt | Post-shunt | |
|---|---|---|
| Transjugular intrahepatic portosystemic shunt | ||
| Portal vein pressure, mmHg (n = 6) | 30 ± 6.5 | 24 ± 8.3 |
| Inferior vena cava pressure, mmHg (n = 6) | 16 ± 2.1 | 17 ± 7.9 |
| PV–IVC pressure gradient, mmHg (n = 6) | 14 ± 4.3 | 8 ± 1.8a |
| H-graft portacaval shunt | ||
| Portal vein pressure, mmHg (n = 9) | 29 ± 8.5 | 29 ± 8.8 |
| Inferior vena cava pressure, mmHg (n = 9) | 13 ± 7.4 | 20 ± 6.7 |
| PV–IVC pressure gradient, mmHg (n = 9) | 16 ± 5.3 | 9 ± 3.5a |
Less than pre-shunt, Wilcoxon matched-pairs test: P < 0.05
Mean pre-shunt SrCR was 1.2 ± 0.769 mg/dl and was not significantly greater than the mean early post-shunt (day 5) SrCr of 0.95 ± 0.585 mg/dl. Mean pre-shunt CrCl was 74 ± 38.3 ml/min and was significantly lower than the mean early post-shunt (postoperative day 5) CrCl of 117 ± 67.07 ml/min (P < 0.05). One year after shunting, mean SrCr (0.93 ± 0.333 mg/dl) was not significantly lower than it had been prior to shunting. Similarly, at 1 year after shunting, mean CrCl (97 ± 48.6 ml/min) was not significantly greater than it had been prior to shunting (Table 3). There were no differences between post-shunt and late (at 1 year) levels of SrCr and CrCl.
Table 3.
Early and late changes in renal function and renal haemodynamics after partial portal decompression
| Serum creatinine, mg/dl | Creatinine clearance, ml/min | Resistive index | Pulsatility index | |
|---|---|---|---|---|
| Pre-shunt | 1.2 ± 0.769 | 74 ± 38.3 | 0.73 ± 0.080 | 1.4 ± 0.412 |
| Post-shunt | 0.95 ± 0.585 | 117 ± 67.07a | 0.76 ± 0.077 | 1.68 ± 0.437a |
| 1 year | 0.93 ± 0.333 | 97 ± 48.6 | 0.72 ± 0.067 | 1.44 ± 0.299 |
Difference to pre-shunt, P < 0.05 (anova matched-samples test)
There were no meaningful differences in mean pre-shunt (P = 0.56), mean post-shunt (P = 0.7) or mean 1 year post-shunt (P = 0.6) SrCr values between the small-diameter HGPCS and TIPS groups. Similarly, there were no differences in mean pre-shunt (P = 0.7), post-shunt (P = 0.9) and 1 year post-shunt (P = 0.4) CrCl values between the groups (Table 4).
Table 4.
Pre-shunt and early and late changes in renal function and renal haemodynamics after H-graft portacaval shunt or transjugular intrahepatic portosystemic shunt
| Serum creatinine, mg/dl | Creatinine clearance, ml/min | Resistive index | Pulsatility index | MELD | |
|---|---|---|---|---|---|
| TIPS (n = 6) | |||||
| Pre-shunt | 1.4 ± 1.2 | 80 ± 54 | 0.7 ± 0.1 | 1.4 ± 0.6 | 16 ± 11 |
| Post-shunt | 1.1 ± 0.9 | 120 ± 79 | 0.8 ± 0.1 | 1.8 ± 0.6 | – |
| 1 year | 1.0 ± 0.4 | 84 ± 14 | 0.7 ± 0.1 | 1.5 ± 0.4 | – |
| HGPCS (n = 9) | |||||
| Pre-shunt | 1.0 ± 0.4 | 70 ± 27 | 0.7 ± 0.1 | 1.4 ± 0.3 | 14 ± 5 |
| Post-shunt | 0.9 ± 0.3 | 116 ± 63 | 0.8 ± 0.1 | 1.7 ± 0.3 | – |
| 1 year | 0.9 ± 0.3 | 105 ± 62 | 0.7 ± 0.04 | 1.4 ± 0.3 | – |
MELD, Model for End-stage Liver Disease; TIPS, transjugular intrahepatic portosystemic shunt; HGPCS, H-graft portacaval shunt
Mean pre-shunt renal artery RI was 0.73 ± 0.08. Mean early post-shunt (postoperative day 5) renal artery RI was 0.76 ± 0.07 (non-significant difference). Mean renal artery RI at 1 year was 0.72 ± 0.067, which was not significantly lower than the pre-shunt value (Table 3). Mean pre-shunt renal artery PI was 1.40 ± 0.412. Mean post-shunt renal artery (postoperative day 5) PI was higher, at 1.68 ± 0.437 (P < 0.05). Mean renal artery PI at 1 year was 1.44 ± 0.299, which was not significantly higher than the pre-shunt value (Table 3). There were no significant differences in mean pre-shunt RI or PI, mean early post-shunt RI or PI, and mean 1-year post-shunt RI or PI between the HGPCS and TIPS groups (Table 4).
Discussion
Renal dysfunction has long been believed to complicate the management of patients with cirrhosis and portal hypertension. Only recently, with the development of MELD, has the importance of renal function on the overall survival of patients with cirrhosis been formally recognized.7 In predicting outcomes of patients with cirrhosis, MELD has been shown to be superior to thetraditional Child–Pugh classification and other systems of risk stratification.8–10 Although the number of patients in this study is small, trends in renal function and perfusion are apparent. Early improvements after shunting in renal function (especially CrCl) and perfusion (especially PI) are generally lost by 1 year after shunting as renal function and perfusion return towards pre-shunt levels. Although renal function is now known to impact survival after portasystemic shunting, this study failed to document a significant beneficial impact of partial portal decompression on renal function and renal haemodynamics in patients with cirrhosis and bleeding varices.
Our patients were mostly older men with advanced alcoholic cirrhosis, who were undergoing portal decompression to treat variceal haemorrhage refractory to or not amenable to sclerotherapy or banding. Prior to shunting, the patients were not in imminent need of or were not eligible for (e.g. because of alcoholism) transplantation. More than 15 patients were enrolled into the study protocol to study liver function after shunting; some died prior to the 1-year follow-up and are excluded from the data analysis. Patients undergoing TIPS or H-graft portasystemic shunting were similar. Ascites, when present, was generally mild and well-controlled with oral diuretics. A minority, although a notable number, had mild encephalopathy before shunting. The patients underwent postoperative study on postoperative day 5 to accommodate haemodynamic changes preceding shunting (e.g. variceal bleeding) and to standardize the day of study after shunting to eliminate untold variables that might complicate renal function or haemodynamics. The patients were all haemodynamically stable at this point. Although none of our patients presented with hepatorenal syndrome, mean SrCr was greater than normal, although not by much, and mean CrCl was nearly half of normal values. In addition, as reported by others,6 our patients demonstrated increased pre-shunt renal arterial tone with elevated RI and PI values. Increased serum levels of aldosterone and angiotensin II, typical in patients with cirrhosis, could and should be responsible for increased renal arterial tone.3 Ultimately, the resulting renal hypoperfusion should be primarily responsible for the impaired renal function seen.
Optimal treatment of severe renal dysfunction in patients with cirrhosis is controversial. Hepatorenal syndrome, acute renal dysfunction in the setting of advanced cirrhosis, has traditionally been treated with medical therapy, including intravenous hydration, generous diuresis, blood products and albumin. In addition, the administration of vasoconstrictors like vasopressin has been associated with a significant improvement in renal function in patients with hepatorenal syndrome.11–14 The improvement in renal perfusion with therapy in hepatorenal syndrome is related to an increase in systemic vascular resistances, a reduction of portal pressure, and the suppression of endogenous vasoconstrictor activity. Furthermore, oral misoprostol, an analogue of prostaglandin E (PGE)-1, has been reported to improve renal dysfunction in patients with cirrhosis, but its application is limited by toxicity.15 Unfortunately, these medications provide temporary rather than durable improvement of extreme renal dysfunction and, generally, are not effective in hepatorenal syndrome. Additionally, prospective studies are lacking.16
Surgical, rather than medical, management has proven to be more efficacious in the treatment of renal dysfunction in patients with cirrhosis. Although liver transplantation represents the definitive treatment for patients with cirrhosis and hepatic induced renal dysfunction, procedural risk, cost, shortage of liver donors, and the potentially high rate of perioperative morbidity in patients suffering pre-transplant renal insufficiency limit the applicability of such therapy.17 Furthermore, patients with cirrhosis and renal dysfunction may otherwise have adequate hepatic reserve and, therefore, not qualify for liver transplantation.
In the early 1970s, isolated reports documented the beneficial effect of portal decompression attained through large-bore, side-to-side portacaval shunts in patients with hepatorenal syndrome. However, these shunts did not become accepted treatment for hepatorenal syndrome because of excessive associated mortality and morbidity.18 The introduction of TIPS has led to the reconsideration of portal decompression to improve renal dysfunction in patients with cirrhosis, particularly in those with hepatorenal syndrome. In the past decade, several reports have documented the relative efficacy of partial portal decompression achieved through TIPS in improving renal function in patients with cirrhosis.19–25 More recently, TIPS has been shown to improve renal perfusion and glomerular perfusion rate and to decrease the activity of vasoactive substances, thereby improving renal function.26 This report adds credibility to those findings by adding to our understanding of the underlying physiology. We believe that the observations contained herein are primarily a result of partial portal decompression and not issues of postoperative management, which is another good reason for studying patients on postoperative day 5 rather than sooner.
In this study, the probability of finding significant changes in renal function and haemodynamics with partial portal decompression was limited by the small number of patients studied. Nonetheless, we found that partial portal decompression, as attained through TIPS or small-diameter prosthetic HGPCS, significantly improved mild to moderate renal dysfunction in patients with cirrhosis. In the early postoperative period, although soon after shunting, mean SrCr was not significantly better than before shunting. CrCl was significantly better than before shunting. However, at 1 year after shunting, CrCl was not significantly better than before shunting as it was found to return towards pre-shunt levels. Interestingly, soon after shunting there was a significant increase in renal arterial tone, with PI values higher than before shunting. Increased renal arterial tone is likely to be related to autoregulation of the renal circulation, which is impacted after shunting by increased cardiac output.27 At 1 year after shunting, renal arterial tone returned to pre-shunt levels, probably as cardiac output decreased towards pre-shunt levels.
Changes in renal function and renal haemodynamics did not differ significantly between patients undergoing TIPS and those undergoing small-diameter HGPCS, presumably because of similarities in the mechanism (i.e. central shunts) and degree of portal decompression. Observations about renal function noted herein reflect the results of perioperative management, variceal blood loss, volume resuscitation and patient care less than the results of partial portal decompression. The partial portal decompression attained through these shunts is a portal vein–inferior vena cava venous fistula and results in increased blood return to the heart with generally increased central venous pressures. The changes in renal function seem to represent a result of portal decompression, given the duration of effect and the fact that patients undergoing either shunt are well by post-shunt day 5, when they are generally ready for discharge. The inclusion of more patients may have led to a statistical difference between renal function at 1 year vs. that before shunting. The inclusion of patients with worse liver function would have relatively minimized the impact of partial portal decompression.
In conclusion, this small, prospective study documents that, in the early period after shunting, partial portal decompression improves mild to moderate renal dysfunction in patients with cirrhosis and bleeding varices with increased venovascular tone. Improvements seen early after shunting are generally lost by 1 year after shunting and, presumably, given enough time, renal dysfunction would completely return to pre-shunt levels.
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