Journal of Hepatology 40 (2004) 228–233
Weight gain after transjugular intrahepatic portosystemic shunt is
associated with improvement in body composition in malnourished
patients with cirrhosis and hypermetabolism
Mathias Plauth1,*, Tatjana Schu¨tz1, Deborah P. Buckendahl1, Georg Kreymann2,
Matthias Pirlich1, Sven Gru¨ngreiff1, Paul Romaniuk3, Siegfried Ertl4,
1Medizinische Klinik mit Schwerpunkt Gastroenterologie, Hepatologie und Endokrinologie, Charite´ Universita¨tsmedizin Berlin, Berlin, Germany
2Medizinische Klinik, Universita¨tsklinikum Hamburg Eppendorf, Hamburg, Germany3Institut fu¨r Ro¨ntgendiagnostik, Charite´ Univerista¨tsmedizin Berlin, Berlin, Germany
4Helios Klinikum Berlin, Klinikum Buch, Nuklearmedizinische Klinik, Berlin, Germany
Background/Aims: To search for changes in body composition and energy metabolism associated with the repeatedly
observed weight gain of cirrhotic patients after portosystemic shunting.
Methods: Twenty-one patients were studied prospectively before and 6 and 12 months after transjugular intrahepatic
portosystemic shunt (TIPS) to assess body cell mass by two independent methods (total body potassium counting: bodycell mass determined by TBP, BCMTBP, bioelectric impedance analysis: body cell mass determined by BIA, BCMBIA),muscle mass (anthropometry), resting energy expenditure (REECALO) by indirect calorimetry, and nutritional intakeby dietary recall analysis.
Results: Prior to TIPS patients were hypermetabolic in terms of measured vs. predicted REE (REECALO median 1423
(range 1164 – 1838) vs. REEPRED 1279 (1067 –1687) kcal; P < 0.05) and their body cell mass was lower (19.1 (10.9 –33.4)vs. 31.7 (16.8 – 47.1) kg; P 5 0.001). After TIPS body cell mass (BCMBIA) increased to 23.5 (12.7 –44.3) (P < 0.025) and25.7 (14.2 – 39.7) kg (P 5 0.05) at 6 and 12 months after TIPS and this was confirmed by total potassium counting(BCMTBP before TIPS: 18.8 (10.6 –26.7) vs. 22.4 (12.9 – 28.5) kg at 6 months; P < 0.01). Hypermetabolism persistedthroughout the study period. Energy and protein intake increased significantly by 26 and 33%.
Conclusions: An increase of prognostically relevant variables body cell and muscle mass contributes to the weight
gain after TIPS in malnourished patients with cirrhosis and hypermetabolism.
q 2003 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.
Keywords: Body cell mass; Nutritional state; Encephalopathy; Protein intake; Bioelectrical impedance analysis
Received 13 February 2003; received in revised form 3 October 2003;
* Corresponding author. Klinik fu¨r Innere Medizin, Staedtisches
Klinikum, Auenweg 38, D-06847 Dessau, Germany. Tel.: þ 49-430-501-
Protein energy malnutrition is a frequent consequence of
hepatic cirrhosis which puts patients at a higher risk of
E-mail address: [email protected] (M. Plauth).
complications , death and a complicated course
Abbreviations: TIPS, transjugular intrahepatic portosystemic shunt; BCM,
after liver transplantation including death After
body cell mass; BCMTBP, body cell mass determined by TBP; TBP, total
successful treatment of portal hypertension by surgical or
body potassium; BCMBIA, body cell mass determined by BIA; BIA,bioelectrical impedance analysis; REE, resting energy expenditure; BMI,
interventional shunt procedures weight gain and improve-
body mass index; MAMA, mid-arm muscle area; MAFA, mid-arm fat area;
ment in the nutritional status have been reported repeatedly
R, resistance; Xc, reactance; FFM, fat-free mass; TBW, total body water;
. In cirrhosis, however, the precise assessment of
TBPMEAS, total body potassium measured values; TBPPRED, total body
nutritional state is complicated by water retention .
potassium content predicted normal values; REECALO, resting energy
Recently, Selberg and coworkers found that the
expenditure measured by indirect calorimetry; REEPRED, resting energyexpenditure predicted from regression equations of healthy controls.
reduction in preoperative body cell mass was a relevant
0168-8278/$30.00 q 2003 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.jhep.2003.10.011
M. Plauth et al. / Journal of Hepatology 40 (2004) 228–233
predictor of a less favourable outcome of liver
Body weight was measured to the nearest 0.1 kg on a hospital scale and
In a prospective study we therefore assessed the
body mass index (BMI) was calculated.
Anthropometric measurements were made at the non-dominant arm
evolution of body composition, energy expenditure, nutrient
using a skinfold caliper (Holtain, Crymych, UK) and a flexible tape
intake, as well as mental state over periods of 6 and 12
measure to calculate mid-arm muscle area (MAMA), mid-arm fat area
months after a transjugular intrahepatic portosystemic stent-
shunt (TIPS) had been inserted As a reference body
Bioelectrical impedance analysis was performed as described else-
where using a BIA 2000-M analyzer (Data Input, Frankfurt/Main,
cell mass estimated by bioelectrical impedance analysis and
Germany) at 50 kHz to measure resistance (R), reactance (Xc) and phase
resting energy expenditure were determined in healthy
angle a. The coefficients of variation for R and Xc were 1.1 and 2.7% in
controls, too. Specifically, we were interested to see: (1)
patients without ascites and 2.1 and 3.9% in patients with ascites. BCM
whether the weight gain following TIPS was associated with
the formulae for fat-free mass (FFM) as TBW/0.732 and total body water
an increase in the metabolically relevant compartments
muscle mass or body cell mass as assessed by two
Total body potassium content (TBP) is being considered a valid
measure of BCM and due to limited access was determined only prior
independent methods; and (2) whether patients with TIPS
to TIPS and after 6 months by measuring the amount of the naturally
do tolerate a diet according to the European Society for
occurring radioisotope 40K using a shielded-room whole-body counter
Clinical Nutrition and Metabolism (ESPEN) guidelines
(Nuclear Enterprises Ltd., Edinburgh, UK) working with four NaI(T1)detectors (Berthold, Wildbad, Germany), as described elsewhere . The
without adverse effects on mental state.
coefficient of variation for repeated measurements was # 2%. BCM wascalculated from TBP as BCM
TBP measurement was not available for the cohort of 310 healthyindividuals. Therefore, measured TBP (TBPMEAS) in cirrhotic patients was
compared with predicted normal values (TBPPRED) calculated from theequations given by McMillan for males as TBP
height) 2 (4.51 £ age) 2 2483 and for females as TBP
Twenty-one patients (13 men, eight women; age: 60.0 (38.7 – 71.6)
years) with liver cirrhosis of alcoholic (n ¼ 19) or non-alcoholic (oneautoimmune hepatitis, one primary biliary cirrhosis) origin were studied
Respiratory gas exchange was measured by indirect calorimetry
prospectively before and 6.0 (5.0 – 7.4) months as well as 12.5 (11.8 – 14.9)
(Deltatrac II, Datex, Bremen, Germany). The intraindividual coefficient
months after TIPS insertion. The indications for TIPS insertion were
of variation of repeated measurements was 3.4% for oxygen consumption
recurrent esophageal variceal bleeding in 14 patients (nine without ascites
and 5.1% for carbon dioxide production. Resting energy expenditure
and five with ascites) and refractory ascites in seven patients. The Child-
(REECALO) was calculated according to Consolazio To search for
Pugh Score was calculated to classify severity of cirrhosis. Of the 21
hypermetabolism in each patient the REECALO was compared to REEPRED
patients included in the study five dropped out after month 6 due to
calculated as a function of measured BCM. REEPRED was calculated from
transplantation (n ¼ 1), death (n ¼ 1), TIPS occlusion (n ¼ 2) and loss to
gender specific regression equations derived from our cohort of healthy
During the initial and follow-up hospitalizations all patients received
dietary counselling according to the ESPEN guidelines Nutritional andmental state were assessed on the occasion of the scheduled visits at months
6 and 12 as part of routine admissions (months 1, 3, 6 and 12 after TIPS
Energy and protein intake of the preceding 2 weeks were assessed prior
insertion) to check for TIPS patency. All patients gave written informed
to TIPS and after 6 months by a standardized diet history (EBISe,
consent for the metabolic study after the indication for the TIPS procedure
Forschungszentrum fu¨r Erna¨hrung, Stuttgart, Germany) Portion sizes
had been established independently and the patients’ consent for the TIPS
of the amount of ingested legumes, potatoes, chips, rice and noodles were
procedure had been obtained. The study protocol conformed to the 1975
estimated by using photographs of four to six portion sizes between 50 and
Helsinki declaration and was approved by the local ethics committee.
A cohort of 310 healthy volunteers consented to have indirect
calorimetry and body composition analysis done by means of bioelectricalimpedance analysis (BIA). From this cohort gender specific regression
equations were derived to calculate expected resting energy expenditure
A battery of six validated psychometric tests (number connection tests
(REE) values for each patient. For the comparison of body cell mass
A and B, digit symbol test, pointing test, line tracing test time and line
determined by BIA (BCMBIA) one healthy individual was matched to each
tracing test mistakes) were performed prior to TIPS insertion as well as 6
patient according to gender and age within ^ 2 years
and 12 months thereafter. In addition to the time needed to execute or thenumber of mistakes the results of each test were classified on a five mark
scale: (þ 1) better than mean þ 1 SD, (0) between mean and mean ^ 1 SD,(2 1) between mean 2 1 SD and mean 2 2 SD, (2 2) between mean 2 2 SDand mean 2 3 SD, and (2 3) less than mean 2 3 SD using age matched
reference values . The global performance of each patient at one testsession was expressed as the average of marks scored in each of the six
TIPS insertion was performed according to the method described by
tests. For follow-up visits four different test arrangements were available to
Ro¨ssle et al. using Memotherme (Angiomed, Karlsruhe, Germany)
devices. There were no intervention associated complications during thefirst 4 weeks. In all patients the TIPS angiography was done 6 months after
TIPS insertion as scheduled, while in seven patients additional angio-graphic interventions were necessary prior to the scheduled one at 6
Results are given as median and range. Statistical analysis was
months. In the whole group reinterventions with dilatation (n ¼ 5) or
performed using the computer software program SPSS (Version 9.0). The
dilatation and insertion of additional stents (n ¼ 10) were required to
Wilcoxon signed rank-sum test was used to compare the values before and
maintain TIPS patency until 6 months and eight reinterventions were
after TIPS insertion as well as between patients before TIPS and controls.
Predicted and measured values were analysed by Mann – Whitney U-test.
M. Plauth et al. / Journal of Hepatology 40 (2004) 228–233
Linear regression analysis based on the control group was used to calculatepredicted values for REE in the study population. Frequencies wereevaluated by the x2-test. Correction for multiple comparisons (6 and12 months after TIPS vs. before TIPS) was performed according toBonferroni with a probability level of less than 0.025 accepted asstatistically significant. Otherwise P , 0:05 was considered statisticallysignificant.
TIPS was well tolerated by all patients. Among the
14 patients in whom TIPS was performed for treatment ofvariceal hemorrhage, there was one episode of varicealbleeding within the first 6 months and one at month 9 due toTIPS occlusion which required a surgical shunt procedure ascompared to 4 (0 – 10) episodes in the year prior to TIPS(P , 0:001) and ascites was absent (n ¼ 4) or moderate(n ¼ 1) in the five patients who also had ascites prior toTIPS. Ascites improved significantly in all seven patients in
Fig. 1. Reduction in body cell mass measured by bioelectricalimpedance analysis (BCM
whom TIPS was performed for treatment of refractory
BIA) in patients (before TIPS) as compared
to age and sex matched controls (C). Gain in BCMBIA of patients at 6
ascites so that ascites grade decreased from a median grade
(TIPS-6) and 12 months (TIPS-12) after TIPS. Box plots with
of 2 (moderate ascites) to a median grade of 1 (no ascites).
horizontal bars indicating median values, boxes indicating the 25th
In fact, none of the patients required further paracenteses.
centiles, error bars indicating the 95% confidence interval and o
TIPS insertion resulted in a persistent reduction of
indicating values outside the 95th centile. ***P < 0.001. [This figureappears in colour on the web.]
portocaval pressure gradient from 23.0 (12 – 29) mmHgprior to TIPS to 15.5 (8 – 21) mm Hg at 6 months(P ¼ 0:002) and 11.5 mmHg at 12 months
Six months after TIPS insertion the patients as a
(P ¼ 0:001) determined on control angiography prior to
group had gained body weight (77.0 (49.0 – 138.5) vs.
any TIPS reintervention. Endogenous creatinine clearance
69.5 (52.0 – 115.0) kg; P ¼ 0:001; weight change 8.0
increased from 94.9 (34.4 – 184.3) ml/min prior to TIPS to
(2 3.7 – 23.5); increase n ¼ 16, stable n ¼ 3, loss n ¼ 2)
98.1 (33.4 – 205.7) ml/min at 6 months and 126.7
reflected by a significant increase in BMI by 11% from
(51.1 – 286.6) ml/min at 12 months (n.s.). Prior to TIPS
22.3 (18.0 – 35.1) to 26.2 (18.3 – 40.0) kg/m2 (P , 0:001).
insertion 67% (14/21) of patients were on diuretics with a
This increase was due to a gain in muscle mass by 18%
median daily dose of oral spironolactone (141.4
in terms of MAMA (48.0 (27.6 – 95.9) vs. 42.6
(21.7 – 88.3) cm2; P ¼ 0:001) or muscle mass as deter-
(5.7 – 80.0) mg, n ¼ 10). At 6 and 12 months, 67 and 44%
mined by the Heymsfield method (23.3 (14.2 – 45.7) vs.
of patients were on diuretics, but at a significantly lower
20.6 (11.4 – 42.7) kg; P ¼ 0:002), while fat mass
daily dose (spironolactone 6 months: 100.0 (42.9 – 142.9)
remained unaltered (MAFA 21.3 (6.7 – 64.9) vs. 23.3
mg, n ¼ 13, P , 0:01; 12 months: 75.0 (50.0– 100.0)
(6.1 – 51.3) cm2). Accordingly, a gain in the metabolically
mg, n ¼ 6, P , 0:01; furosemide 6 months: 40.0
active compartment body cell mass could be demon-
(2.9 – 80.0) mg, n ¼ 11, P , 0:025; 12 months: 30.0
strated by two independent methods: bioelectrical impe-
(20.0 – 80.0) mg, n ¼ 6, P , 0:01).
dance analysis (BCMBIA: 23.5 (12.7 – 44.3) vs. 19.1(10.9 – 33.4) kg; þ 15%; P , 0:025) and total body
potassium counting (BCMTBP 22.2 (12.9 – 28.5) vs. 18.8(10.6 – 26.7) kg; þ 15%; P , 0:01; BCMTBP even
Weight 69.5 (52.0 – 115.0) vs. 74.0 (45.0 – 115.0) kg,
increased to the level of predicted normal values
height 170 (158 – 185) vs. 171 (152 – 185) cm) and body
(87 ^ 5%; ns) at 6 months, as opposed to 77 ^ 5%
mass index 22.3 (18.0 – 35.1) vs. 25.6 (16.9 – 37.4) kg/m2)
prior to TIPS (P , 0:01), again showing a significant
were not different between patients and controls. However,
improvement (P , 0:01) after TIPS insertion ().
patients with cirrhosis showed a significant reduction in
In the subgroup of 16 patients also studied 12 months
metabolically relevant lean tissue, both in terms of body cell
after TIPS insertion, a persistent gain in weight of 0.9
mass (BCMBIA 19.1 (10.9 – 33.4) vs. 31.7 (16.8 –47.1) kg;
(2 9.1 – 8.0) to (72.7 (54.0 – 142.6) kg; P , 0:01), body
P ¼ 0:001, calculated from impedance measure-
mass index (25.8 (20.6 – 42.6) kg/m2; P , 0:025), arm
ments and in terms of the directly measured variable phase
muscle area (16.8 (9.7 – 69.8) cm2; P , 0:001) and body cell
angle a (4.5 (2.9 – 6.2)8 vs. 6.5 (5.8 – 7.5)8; P , 0:001) when
mass (BCMBIA 25.7 (14.2 – 40.0) kg, n.s., ; phase
compared to age and gender matched controls.
angle a 5.2 (3.8 – 6.0)8, n.s.) could be demonstrated.
M. Plauth et al. / Journal of Hepatology 40 (2004) 228–233
(P , 0:025). Measured REECALO remained higher thanpredicted values REEPRED at 6 months (1550 (1203 – 2364)vs. 1402 (1112 – 2000) kcal/d; P ¼ 0:001) and 12 months(1532 (1208 – 2232) vs. 1465 (1152 – 1868) kcal/d;P , 0:05) after TIPS, but the initial difference decreasedduring follow-up.
Total energy intake before TIPS was 1842 (1334 – 3687)
kcal/d and increased by 6 months after TIPS by 26% to 2533(1014 – 4062) kcal/d (P , 0:05). This was due to an increasein protein (1.2 (0.7 – 1.7) g kg21 d21 vs. 0.9 (0.5 – 1.2) gkg21 d21; P ¼ 0:05) and carbohydrate intake (3.7 (2.0–5.4)g kg21 d21 vs. 2.9 (1.7 – 4.9) g kg21 d21; P ¼ 0:05), while
Fig. 2. Reduction in body cell mass (BCMTBP) assessed by total body
fat intake remained unchanged (1.4 (0.6 – 2.0) g kg21 d21
potassium counting in patients before TIPS. Patient values are
compared to predicted normal values calculated according toMcMillan Six months after TIPS BCMTBP has increased
significantly and is no longer different from predicted values. Legendsand box plot as explained in **P < 0.01. [This figure appears incolour on the web.]
The majority of patients (63 – 95% before TIPS and
47 – 95% after TIPS) performed below the limit (age
adjusted mean minus two standard deviations) in individualpsychometric tests with the exception of line tracing errors,
Before TIPS patients had a measured total body
but not time. After TIPS, there were significant improve-
ments in the number connection test B (P ¼ 0:001) at month
CALO of 1449 (1164 – 1838) kcal/d which was lower
than in matched controls (1644 (1117 – 2181) kcal/d;
6 and the pointing test at months 6 and 12 (P , 0:01 and
P , 0:05). However, when the patients’ energy expenditure
P , 0:025) In terms of global performance,
was calculated using the regression equations, their
however, there was no improvement after TIPS (n.s.).
predicted metabolic rate REEPRED (1279 (1067 – 1687)kcal/d was significantly lower than the measured REECALO1423 (1164 – 1837) kcal/d; P , 0:05; indicating
In this prospective study we demonstrated that body cell
mass in patients with liver cirrhosis is severely reduced andthis condition does not inevitably run a downhill course butcan be ameliorated as demonstrated in a patient cohorttreated with TIPS. Using three independent methods(anthropometry, bioelectrical impedance analysis, totalbody potassium counting) to analyse body composition wecould not only confirm the repeatedly claimed improvementin nutritional state after successful portosystemic shuntingbut also show that this improvement is associated with again in the metabolically relevant compartments musclemass (anthropometry) and body cell mass (bioelectricimpedance analysis and total body potassium counting). As would be expected, this gain in lean body mass was notcorrelated with weight change since improvement of ascites
Fig. 3. Hypermetabolism in liver cirrhosis before TIPS and at 6
was observed after TIPS as well. BCM is the sub-
(TIPS-6) and 12 (TIPS-12) months after TIPS. Resting energy
compartment of lean body mass, in which 99% of the
expenditure was measured by indirect calorimetry (REECALO) and
body’s metabolic processes take place , and significant
values are compared with predicted REEPRED from actual BCM using
losses of which are tightly linked to mortality . The
regression equations of healthy volunteers (for details see text).
fact that the improvement in nutritional state was more
Legends and box plot as explained in . *P < 0.05, ***P 5 0.01. [This figure appears in colour on the web.]
readily observed in our patient population but only less so in
M. Plauth et al. / Journal of Hepatology 40 (2004) 228–233
Table 1Overview of psychometric tests results before and 6 and 12 months after TIPS
Values are median (range). Results were available for statistical analysis in 19/21 or 15/16 patients due to test termination prior to maximum time (# one
another study may be related to the degree of
counselling, unless supplemental artificial feeding provides
malnutrition prior to TIPS insertion as reflected by
additional energy and protein . We were pleased to
the severe reduction in BCM in our patients. As shown
see that, after TIPS insertion patients managed to increase
recently there is reasonable agreement between BIA
total energy (þ 26%) and protein intake (þ 33%) and
and TBP counting regarding the determination of BCM
reached a stable anabolic state without any nutritional
even in cirrhotic patients with massive ascites. Body cell
intervention apart from dietary counselling. This obser-
mass calculation from TBP or BIA data is based on
vation shows that in a group of patients with predominantly
assumptions which may not be fully adequate in cirrhosis
repeated variceal hemorrhage receiving TIPS as salvage
and, therefore, it is important to see the major result of the
therapy the loss of BCM does not inevitably progress but
study confirmed by independent methodology, such as an
can actually be stopped and reverted to increase. Whether
increase in muscle mass and the recent findings of
this favourable change was causally related to TIPS cannot
be answered from the present data. One may speculate,however, that the treatment of portal hypertension may have
improved intestinal nutrient absorption, food intake due torelief from abdominal fullness, or protein anabolism after a
Searching for changes in energy metabolism as a
prolonged period without catabolic insults from hemorrhage
potential cause for the improvement of nutritional status,
or paracenteses. It is conceivable that the absence of a
we observed an increase in total resting energy expenditure
worsening in mental state in our cohort of patients with
REECALO following TIPS and this occurred irrespective of
psychometrically diagnosed subclinical encephalopathy is a
the presence of ascites prior to TIPS To correct for the
result of pro-encephalopathic interventions like TIPS on the
effects of changes in BCM we related REECALO to
one hand and anti-encephalopathic interventions like
REEPRED predicted from the measured BCM of each patient
adequate nutrition with a 33% percent increase in protein
using regression equations derived in the group of 310
consumption on the other hand. This would not be
healthy controls. We chose this approach to allow for the
surprising since controlled trials feeding high protein diets
curvilinear relationship between REE and BCM instead
to patients with liver cirrhosis have generated
of expressing this relationship as the ratio of REE/BCM
sound data to dismiss protein intolerance as a dangerous
which may erroneously overestimate REE in individuals
myth rather than a clinically relevant pathogenic principle
with low BCM. This analysis revealed hypermetabolism in
patients prior to TIPS which persisted throughout the
We conclude that even malnourished patients with liver
observation period of 12 months but showed a tendency to
cirrhosis and hypermetabolism are capable to improve their
decrease. This observation may reflect the ongoing chronic
lean body mass and this increase of prognostically relevant
liver disease and the TIPS associated augmentation of
variables body cell and muscle mass contributes to the
portalsystemic shunting on the one hand and the improved
nutrient balance on the other hand which requires long-termrather than short-term follow-up to detect an improvementof body composition.
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Rede von Annette Widmann-Mauz Parlamentarische Staatssekretärin beim Bundesminister für Gesundheit Mitglied des Deutschen Bundestages „Pille danach“ anlässlich der Parlamentsdebatte am 13. Februar 2014 in Berlinwir debattieren heute über verschiedene Anträge der Oppositionsfraktionen mit dem Ziel, denArzneimittelwirkstoff Levonorgestrel – eine Variante der „Pil e dana
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