Measuring resting energy expenditure during extracorporeal membrane oxygenation: Preliminary clinical experience with a proposed theoretical model

Abstract

Extracorporeal membrane oxygenation (ECMO) is increasingly used in patients with severe respiratory failure. Indirect calorimetry (IC) is a safe and non-invasive method for measuring resting energy expenditure (REE). No data exist on the use of IC in ECMO-treated patients as oxygen uptake and carbon dioxide elimination are divided between mechanical ventilation and the artificial lung. We report our preliminary clinical experience with a theoretical model that derives REE from IC measurements obtained separately on the ventilator and on the artificial lung.
A patient undergoing veno-venous ECMO for acute respiratory failure due to bilateral pneumonia was studied. The calorimeter was first connected to the ventilator and oxygen consumption (VO2 ) and carbon dioxide transport (VCO2 ) were measured until steady state was reached. Subsequently, the IC was connected to the membrane oxygenator and similar gas analysis was performed. VO2 and VCO2 values at the native and artificial lung were summed and incorporated in the Weir equation to obtain a REEcomposite .
At the ventilator level, VO2 and VCO2 were 29.5 ml/min and 16 ml/min. VO2 and VCO2 at the artificial lung level were 213 ml/min and 187 ml/min. Based on these values, a REEcomposite of 1703 kcal/day was obtained. The Faisy-Fagon and Harris-Benedict equations calculated a REE of 1373 and 1563 kcal/day.
We present IC-acquired gas analysis in ECMO patients. We propose to insert individually obtained IC measurements at the native and the artificial lung in the Weir equation for retrieving a measured REEcomposite .
© 2015 The Acta Anaesthesiologica Scandinavica Foundation. Published by John Wiley & Sons Ltd.

Full text

Measuring resting energy expenditure during extracorporeal
membrane oxygenation: preliminary clinical experience with a
proposed theoretical model
E. De Waele
1
, K. van Zwam
2
, S. Mattens
1
, K. Staessens
2
, M. Diltoer
1
, P. M. Honor
e
1
, J. Czapla
2
, J. Nijs
2
,
M. La Meir
2
, L. Huyghens
1
and H. Spapen
1
1
Intensive Care Department, Universitair Ziekenhuis Brussel (UZ Brussel), Vrije Universiteit Brussel (VUB), Brussels, Belgium
2
Department of Cardiac Surgery, Universitair Ziekenhuis Brussel (UZ Brussel), Brussels, Belgium
Correspondence
E. De Waele, Intensive Care Department,
Universitair Ziekenhuis Brussel (UZ Brussel),
Vrije Universiteit Brussel (VUB), Brussels,
Belgium
E-mail: elisabeth.dewaele@uzbrussel.be
Conflicts of interest
All authors declare no potential or actual
personal, political, or financial interest in the
material, information, or techniques described
in the paper.
Funding
The study received no funding.
Submitted 13 April 2015; accepted 6 May
2015; submission 25 February 2015.
Citation
De Waele E, van Zwam K, Mattens S,
Staessens K, Diltoer M, Honor
e PM, Czapla J,
Nijs J, La Meir M, Huyghens L, Spapen H.
Measuring resting energy expenditure during
extracorporeal membrane oxygenation:
preliminary clinical experience with a
proposed theoretical model. Acta
Anaesthesiologica Scandinavica 2015
doi: 10.1111/aas.12564
Background: Extracorporeal membrane oxygenation (ECMO) is
increasingly used in patients with severe respiratory failure. Indi-
rect calorimetry (IC) is a safe and non-invasive method for mea-
suring resting energy expenditure (REE). No data exist on the use
of IC in ECMO-treated patients as oxygen uptake and carbon
dioxide elimination are divided between mechanical ventilation
and the artificial lung. We report our preliminary clinical experi-
ence with a theoretical model that derives REE from IC measure-
ments obtained separately on the ventilator and on the artificial
lung.
Methods: A patient undergoing veno-venous ECMO for acute
respiratory failure due to bilateral pneumonia was studied. The
calorimeter was first connected to the ventilator and oxygen con-
sumption (VO
2
) and carbon dioxide transport (VCO
2
) were mea-
sured until steady state was reached. Subsequently, the IC was
connected to the membrane oxygenator and similar gas analysis
was performed. VO
2
and VCO
2
values at the native and artificial
lung were summed and incorporated in the Weir equation to
obtain a REE
composite
.
Results: At the ventilator level, VO
2
and VCO
2
were 29.5 ml/
min and 16 ml/min. VO
2
and VCO
2
at the artificial lung level
were 213 ml/min and 187 ml/min. Based on these values, a
REE
composite
of 1703 kcal/day was obtained. The Faisy–Fagon and
Harris–Benedict equations calculated a REE of 1373 and
1563 kcal/day.
Conclusion: We present IC-acquired gas analysis in ECMO
patients. We propose to insert individually obtained IC measure-
ments at the native and the artificial lung in the Weir equation for
retrieving a measured REE
composite
.
Editorial comment: what this article tells us
Measurement or estimation of energy expenditure may be helpful in dosing the caloric part of
nutrition. Extracorporeal oxygenation and carbon dioxide removal are techniques applied to an
increasing number of critically ill patients. Here, the authors address how to manage this chal-
lenge.
Acta Anaesthesiologica Scandinavica (2015)
ª2015 The Acta Anaesthesiologica Scandinavica Foundation. Published by John Wiley & Sons Ltd 1
ORIGINAL ARTICLE

Indirect calorimetry (IC) is currently considered
to be the method of choice for determining rest-
ing energy expenditure (REE) in critically ill
patients.
1
IC allows quantification of REE by
measuring oxygen consumption (VO
2
) and car-
bon dioxide transport (VCO
2
) from in- and
exhaled air gases. Most IC systems use the mod-
ified Weir equation to calculate metabolic
rate.
2,3
Extracorporeal membrane oxygenation (ECMO)
provides a pump-driven lung or heart-lung
bypass support. Gas exchange occurs both in
the native and in an artificial lung. The latter is
conceived as an external membrane oxygenator
consisting of a thin gas-permeable membrane
separating the blood and gas flows in the car-
diopulmonary bypass circuit. Over this mem-
brane, oxygen (O
2
) is supplied through
diffusion from the gas side into the blood, while
carbon dioxide (CO
2
) is disposed from the
blood into the gas. In the intensive care unit
(ICU), ECMO is used as a “last stage” therapeu-
tic option to support cardiac and/or respiratory
function in patients with intractable heart fail-
ure or severe lung damage. In particular, ECMO
is increasingly applied in patients with the
adult respiratory distress syndrome.
4
Metabolic rate has been shown to vary widely
over time in and among neonates treated with
ECMO.
5,6
This emphasizes the need for individ-
ual REE assessment to guide nutritional therapy
and to prevent over- and underfeeding. However,
definite feeding instructions adapted to the energy
needs of adult ECMO patients are not available.
Expert opinion recommends to follow nutrition
guidelines that are applicable in a general popula-
tion of critically ill subjects.
7
This would also
imply the use of IC
2
, but this technique has not
been studied in an adult ECMO setting.
We present a method to perform IC and pro-
pose a theoretical model for evaluating REE
during ECMO. Preliminary experience with this
approach in a patient is described.
Methods
We studied a 60-year-old female ICU patient with
pneumonia-induced severe respiratory failure
necessitating initiation of veno-venous ECMO
treatment. The study was in compliance with the
declaration of Helsinki and approved by the Hos-
pital’s Institutional Review Board. The need for
informed consent was waived because IC is part
of daily clinical routine in our ICU and nutrition
therapy is protocol-based in accordance with offi-
cial guidelines. The Review Board strictly stipu-
lated that ECMO should be adapted to the
patient’s condition and evolution and not to study
purposes.
Patient, IC, and ECMO arrangements during
the study are depicted in detail in Fig. 1. Fol-
lowing hemodynamic stabilization, ventilator
settings were: tidal volume 160 ml; respiratory
Fig. 1. Schematic representation of patient, indirect calorimeter, and
ECMO system. 1 =indirect calorimeter in position 1; 2 =outflow
sampler, 3 =inflow sampler, 4 =outflow of mechanical ventilator,
5=oxygen/air, 6 =mechanical ventilator (including internal circuit),
7=inspiratory tubing, 8 =expiratory tubing, 9 =endotracheal tube,
10 =venous return tubing ECMO, 11 =indirect calorimeter in position
2, 12 =outflow sampler, 13 =inflow sampler, 14 =outflow of
oxygenator, 15 =inflow of oxygenator, 16 =ECMO 17 =pump,
18 =oxygenator, 19 =return cannula, 20 =ECMO tubing,
21 =venous drainage cannula, 22 =inferior vena cava.
Acta Anaesthesiologica Scandinavica (2015)
2ª2015 The Acta Anaesthesiologica Scandinavica Foundation. Published by John Wiley & Sons Ltd
E. DE WAELE ET AL.

rate 26/min; peak inspiratory pressure
28 cmH
2
O; PEEP 13 cmH
2
O; and FiO
2
35%.
Venous access for ECMO was provided by a
25Fr femoral cannula for venous drainage and a
19Fr jugular cannula for blood return. ECMO
settings, adapted to blood gases, were: flow rate
3.2 l/min; gas flow 3.5 l/min, and FiO
2
100%.
Sweep gas flow was provided and determined
by an equilibrated gas blender, verified for
accuracy (<1% difference) by repeated compari-
son with measurements obtained by a mass
flow meter (TSI Mass Flowmeter, 4040; Shore-
view, MN, USA). The ECMO (Eurosets

, Medo-
lla, Italy) was operated by a perfusionist under
permanent supervision of the attending ICU
physician and the senior researcher. The ECMO
oxygenator was equipped with a long-term,
non-porous 1.81 m
2
polymethylpentene mem-
brane and a phosphorylcholine-coated anti-
thrombotic tubing set. An inflow analyzer was
connected to the gas inlet line of the oxygenator.
A custom-made 3/8 inch silicone tube was used
to fix the outflow analyzer on the outflow tract
of the oxygenator. This construction prevented
room air from entering the measuring canal and
thus permitted to capture only the gas flow
emanating from the oxygenator. Heat exchanger
(3T Heater Cooler system

; Sorin Group, Arva-
da, CO, USA) temperature was set standard at
37°C aiming at a core body temperature of
36 0.5°C. Heat exchange was guaranteed by a
10 l/min water flow over the 0.08 m
2
heat
exchange unit of the oxygenator (performance
factor 0.64 at 4 l/min). Higher temperature set-
tings were avoided for safety reasons as this
might induce hyperthermia, increased oxygen
consumption, and denaturation of plasma pro-
teins. Room and body temperature as well as
thermoregulation were permanently monitored.
The Vmax Encore 29n (VIASYS Healthcare Inc,
Yorba Linda, CA, USA) indirect calorimeter was
used to measure REE. This calorimeter is an
open-circuit system equipped with an infrared
CO
2
and an electrochemical O
2
sensor and uses
breath-by-breath technology. Expiratory flow
was measured by a mass flow sensor placed on
the expiratory outlet of the ventilator. The calo-
rimeter was calibrated before measurement.
8
VO
2
and VCO
2
were adjusted to standard tem-
perature (273 K) and pressure (1013 hPa) dry
•Weir : heat output (kg.cal) = 3.94 x L O2used + 1.11 x L CO2produced (ref. 2)
•Weirabbr : REE = (3.94 x VO2) + (1.11 x VCO2) x 1440
REEcomposite = (3.94 x VO2 total) + (1.11 x VCO2 total) x 1440 (ref. 13)
VO2 total = VO2 native lung + VO2 ECMO
VCO2 total = VCO2 native lung + VCO2 ECMO
VO2
VO2
ECMO = (FiO2 ECMO x VI ECMO) – (FeO2 ECMO x VE ECMO) (ref. 26)
VCO2 ECMO = (FeCO2 ECMO x VE ECMO) – (FiCO2 ECMO x VEECMO)
VCO2 native lung = (FeCO2 x VEnative lung) – (FiCO2 x VEnative lung)(ref. 23)
native lung = VE x (FiO2 –Fe
O2)(ref. 23)
REE: Resting Energy Expenditure (kCal/24 h)
VO2 : Oxygen transfer (L/min)
VCO2 : carbon dioxide transfer (L/min)
FiO2 : fractional concentration of oxygen in inspired air *
FeCO2 : fractional concentration of carbon dioxide in expired air *
VI : Volume of inspired air (L/min)*
VE : Volume of expired air (L/min)*
Fig. 2. Formulas used to retrieve resting
energy expenditure during ECMO.
Acta Anaesthesiologica Scandinavica (2015)
ª2015 The Acta Anaesthesiologica Scandinavica Foundation. Published by John Wiley & Sons Ltd 3
INDIRECT CALORIMETRY DURING ECMO

conditions and expressed in ml/min.
9
IC installa-
tion, calibration, and measurements were
performed by the same experienced investigator.
The IC tubing was first connected to the in- and
outflow limbs of the ventilator. Measurements
were performed until steady state was reached,
discarding the initial 5 min and aiming at ≤5%
VO
2
and VCO
2
variability over a 5-min period.
9
Data were recorded at a frequency of one read-
out/min. Subsequently, the IC was connected to
the artificial lung with a specifically designed
connector, custom-made by our institutional
engineers, and gas analysis executed at the oxy-
genator in- and outflow tract. After 35 min, a
dataset with least variability was obtained. Any
treatment changes or adaptations, patient manip-
ulation, or nursing procedures were not allowed
during IC measurement. Overall, the patient
remained under continuous hemodynamic, neu-
rological, and respiratory monitoring.
The acquired gas transfer data were summed
and imported into the Weir equation to retrieve
REE (REE
composite
) (Fig. 2). IC measurements
obtained at the artificial lung were then substi-
tuted by the gas transfer characteristics of the
membrane oxygenator as specified in the manu-
facturer’s manual, i.e., a VO
2
of 220 ml/min and
aVCO
2
of 180 ml/min at a gas flow of 3.5 l/min.
The Weir equation was recalculated accordingly
(Fig. 3). Finally, REE was calculated from two
commonly used equations [Faisy–Fagon: REE
(kcal/d) =89body weight (kg) +14 9height
(cm) +32 9minute ventilation (l/min) +94 9
body temperature (°C) 4834; Harris–Benedict
1984 (for female patient): REE (kcal/
d) =447.593 +(9.247 9weight (kg)) +(3.098 9
height (cm)) (4.33 9age (y)] and from the
ESPEN guideline (25 kcal/kg/day).
1,2,11–13
Results
IC measurements at the ventilator level (n=29) were:
volume of expired air, 4.22 0.335 l/min; fractional
concentration of O
2
in inspired (FiO
2 native lung
)and
expired air (FeO
2 native lung
), 34.51 0.1957% and
33.79 0.1609%; fractional concentration of CO
2
in
inspired
(FiCO
2 native lung
) and expired air (FeCO
2native
lung
), 0.051 0.0026% and 0.429 0.0191%. Net
O
2
transfer over the native lung (VO
2nativelung
)was
29.5 ml/min and net CO
2
transfer over the native
lung (VCO
2 native lung
) was 16 ml/min.
Measurements at the artificial lung level (n=35)
were: fractional concentration of O
2
in inflow air
(FiO
2ECMO
) and exhaust gas (FeO
2ECMO
),
95.01 0.2309% and 88.87 0.2834%; and frac-
tional concentration of CO
2
in inflow air (FiCO
2
ECMO
) and in exhaust gas (FeCO
2ECMO
),
0.053 0.011% and 5.39 0.133%. Net trans-
membranous O
2
(VO
2ECMO
)andCO
2
(VCO
2ECMO
)
transfer were 213 ml/min and 187 ml/min.
Applying the Weir formula on the combined
data produced a REE
composite
of 1703 kcal/day.
Implementing the manual-derived VO
2
and
VCO
2
membrane oxygenator characteristics
into the Weir formula retrieved a REE of
1729 kcal/day. The Faisy–Fagon and Harris–
Benedict equations yielded REE values of 1373
and 1563 kcal/d.Application of the ESPEN
guideline estimated REE in our patient at
1675 kcal/d.
Discussion
We describe an original and user-friendly set-
ting enabling metabolic cart measurement in
ECMO patients. We also propose a method for
estimating REE under ECMO conditions.
According to this method, respiratory gas
exchange analysis is done separately at the ven-
tilator and at the artificial lung. The data are
then combined and introduced in the modified
Weir equation to obtain REE. As documented
earlier,
14
formula-based calculations of REE
were not mutually consistent and underesti-
mated REE by approximately 10–20% as com-
pared with measured REE values.
The number of critically ill patients receiving
prolonged ECMO therapy is increasing over the
years.
15
Sufficient calories and proteins must be
Weir ECMOoxyg : REE = {(3.94 x VO2 total ) + (1.11 x VCO2 total)} x 1440
VO2 total = VO2 native lung + VO2 ECMOoxyg
VCO2 total = VCO2 native lung + VCO2 ECMOoxyg
VO2 ECMOoxyg and VCO2 ECMOoxyg derived from oxygenator’s characteristics
Fig. 3. Formula used to retrieve resting energy expenditure during
ECMO by using oxygenator gas transfer characteristics at a gas flow
of 3.5 l/min.
Acta Anaesthesiologica Scandinavica (2015)
4ª2015 The Acta Anaesthesiologica Scandinavica Foundation. Published by John Wiley & Sons Ltd
E. DE WAELE ET AL.

supplied to avoid excessive muscle wasting and
prevent further tissue damage. However, esti-
mating energy needs in ECMO patients remains
challenging.
16
Nutrition guidelines are available
for neonates and children supported with
ECMO. It is known, for instance, that a surplus
of dietary caloric intake in this particular popu-
lation does not improve protein catabolism and
increases CO
2
production.
17
In contrast, data on
energy requirements and handling of nutrition
in adults undergoing ECMO are scant.
18
Even
an international consortium of ECMO experts
remains vague by stating only “to guarantee full
caloric and protein nutritional support” but
without specifying how this should be accom-
plished.
19
A recent study in adult transplant
patients receiving ECMO merely recommended
to feed them as any other critically ill patient.
7
However, nutritional adequacy defined as the
ratio of delivered nutrition to target nutrition
(calculated with the Schofield equation cor-
rected for stress) was found to be disappoint-
ingly low (55%) under ECMO treatment.
20
Several studies have highlighted the impor-
tance of IC to guide nutrition in critically ill
patients. When technically feasible, IC may be a
valid alternative for the nutritional mayhem
caused by the overwhelming number of formu-
las and equations used for calculating REE.
14
Moreover, optimizing energy needs according to
an IC-based protocol has been shown to
improve outcome in critically ill patients.
21,22
The use of IC is also the main reason to
explain why energy needs are better appreciated
in neonates and infants. In fact, a closed-circuit
IC technique adapted to quantitate gas exchange
across the native lung and the membrane oxy-
genator in neonatal ECMO was already devel-
oped three decades ago. This allowed to
estimate REE over time and among neonates,
improved evaluation of pulmonary recovery,
and facilitated weaning from ECMO.
6,23
Mea-
sured REE varied widely over time and among
neonates. By using a technique comparable with
our setup but in venoarterial ECMO mode,
Shanbhogue proved a significant relationship
between ECMO flow and gas exchange across
the membrane and lungs in neonates.
24
Since
then, other IC applications and refinements
adapted to different ventilation conditions and/
or pediatric populations have been validated.
25
The proposed model remains theoretical, and
the intertwining of physiological and mathemat-
ical principles is debatable. As such, several
shortcomings and limitations must be under-
lined. IC measurements on ventilator and oxy-
genator were performed only once over a 70-
min period at one readout/min. This precluded
evaluation of energy requirements over time.
Oxygenator outflow gas was only partly ana-
lyzed because the outflow valve was not
occluded. However, creating outflow resistance
is hazardous because it may increase the risk for
developing air emboli. In the absence of a
golden “ECMO-IC” standard, the accuracy of
our VO
2
and VCO
2
measurements could be
challenged. Therefore, we chose to determine
the precision of our method by recording the
variability in repeated measurements. All 64
measurements taken together, precision was
estimated to be sufficiently high as reflected by
the small standard deviations. The validity of
VO
2
/VCO
2
calculations from unidirectional flow
measurements without using the Haldane trans-
formation equation could be argued. However,
this equation describes the mathematical expres-
sion of the relationship between inspiratory and
expiratory air in a respiratory circuit within lim-
its of FiO
2
and has not been validated in an
ECMO setting. Recirculation of blood within
the venous system might have confounded
results. This is probably of minor importance as
patient, mechanical ventilator, and artificial lung
formed a closed system during measurements.
As observed in continuous renal replacement
therapy (CRRT), metabolic cart measurements
may be blurred by a significant loss of calories
due to passage of blood through an external cir-
cuit. However, CRRT functions at low flow rates
with longer extracorporeal exposure time result-
ing in more heat loss and higher REE, whereas
heat transfer within a high flow ECMO system
is less pronounced and active rewarming of the
oxygenator up to 37°C precludes any substantial
calorie loss. Adjusting core body temperature to
the temperature set at the heat exchanger will
induce an increase in metabolic rate measured
by the calorimeter as an increase in CO
2.
Simul-
taneous rather than consecutive IC measurement
would have been a more correct approach. Yet,
this was logistically difficult as we had only one
metabolic cart available. The ECMO gas flow
Acta Anaesthesiologica Scandinavica (2015)
ª2015 The Acta Anaesthesiologica Scandinavica Foundation. Published by John Wiley & Sons Ltd 5
INDIRECT CALORIMETRY DURING ECMO

values used in the Weir formula were derived
from oxygenator settings after IC calibration.
The REE was calculated using the membrane
oxygenator characteristics. Overall, as the Vmax
Encore n29 –and by extension all commercial-
ized ICs –shows variation in measurements,
any individual measurement is uncertain to an
unknown extent.
9
Finally, the oxygenator’s
membrane polymethylpentene fibers were validated
for bovine blood
26
and thus could have influenced
gas exchange differently in human blood. However,
hemoglobin O
2
and CO
2
charges, albeit different in
the two species, will not influence the diffusion
gradient. The latter indeed depends only on O
2
and
CO
2
dissolved in human or bovine blood which is
physiologically similar. Preliminary clinical experi-
ence with the ECMO system used in our patient
confirmed efficient transmembranous gas
exchange.
27
In addition, we found only marginal
difference in REE
composite
when either measured or
manual-specified VO
2
and VCO
2
values were
implemented in the Weir formula.
Conclusion
We present a theoretical model based on a bi-
level (native and artificial lung) IC measurement
of REE in an ECMO setting and report its first
clinical use. Many imperfections, uncertainties,
and eventual incongruities of this novel
approach are acknowledged. Further prospective
research in a larger group of patients is neces-
sary to settle outstanding questions and contro-
versy and to determine whether this model may
contribute to a more optimal metabolic and
nutritional approach of the critically ill patient
requiring ECMO.
Authors’ contribution
All authors have made substantial contributions
to the paper and have read and approved its
final version.
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Acta Anaesthesiologica Scandinavica (2015)
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INDIRECT CALORIMETRY DURING ECMO