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Thorax 2002;57(Suppl II):ii47–ii52
PREOPERATIVE PREDICTORS OF
OUTCOME FOLLOWING LUNG
VOLUME REDUCTION SURGERY *
ii47
F C Sciurba
Original article
Patients at high risk of death after lung-volume-reduction
surgery
The National Emphysema Treatment Trial Research Group
Background: Lung-volume-reduction surgery is a proposed treatment for emphysema, but
optimal selection criteria have not been defined. The National Emphysema Treatment Trial
is a randomized, multicenter clinical trial comparing lung-volume-reduction surgery with
medical treatment. Methods: After evaluation and pulmonary rehabilitation, we randomly
assigned patients to undergo lung-volume-reduction surgery or receive medical treatment.
Outcomes were monitored by an independent data and safety monitoring board. Results:
A total of 1033 patients had been randomized by June 2001. For 69 patients who had a
forced expiratory volume in one second (FEV1) that was no more than 20% of their predicted value and either a homogeneous distribution of emphysema on computed tomography or a carbon monoxide diffusing capacity that was no more than 20% of their predicted
value, the 30-day mortality rate after surgery was 16% (95% confidence interval, 8.2 to
26.7), as compared with a rate of 0% among 70 medically treated patients (p<0.001).
Among these high-risk patients, the overall mortality rate was higher in surgical patients
than medical patients (0.43 deaths per person-year vs. 0.11 deaths per person-year; relative risk, 3.9; 95% confidence interval, 1.9 to 9.0). As compared with medically treated
patients, survivors of surgery had small improvements at six months in the maximal workload (p=0.06), the distance walked in six minutes (p=0.03), and FEV1 (p<0.001), but a
similar health-related quality of life. The results of the analysis of functional outcomes for
all patients, which accounted for deaths and missing data, did not favor either treatment.
Conclusions: Caution is warranted in the use of lung-volume-reduction surgery in patients
with emphysema who have a low FEV1 and either homogeneous emphysema or a very low
carbon monoxide diffusing capacity. These patients are at high risk for death after surgery
and also are unlikely to benefit from the surgery. (N Engl J Med 2001;345:1075–83)
M
F C Sciurba
Associate Professor of
Medicine, Division of
Pulmonary and Critical
Care Medicine, University
of Pittsburgh, Pittsburgh,
PA 15213, USA;
[email protected]
ore than 8 years after the resurrection of lung volume reduction surgery (LVRS), significant controversy continues to surround many aspects of this procedure.1–7 The
procedure unquestionably results in short term improvement in a significant number of
patients. However, the proportion of patients with suYcient short and long term improvement and
the overall morbidity continues to be controversial. An issue central to the variable acceptance of
LVRS is the need for more objective definitions of those preoperative characteristics that determine
the degree of physiological benefit and those which define the morbidity following the procedure.
The Introductory article from the National Emphysema Treatment Trial (NETT) Research
Group8 identifies preoperative characteristics that define two subsets of subjects at particularly high
risk of perioperative mortality. The analysis emerged in the context of the periodic reviews by the
NETT data safety and monitoring board (DSMB), a group charged with identifying indices associated with disproportionate morbidity or benefit. The two subgroups identified by the DSMB in
this report represented 140 of the 1033 randomised subjects who were found to exceed a 30 day
surgical mortality rate of 8%, the value (95% lower confidence limit) identified a priori as a stopping guideline.
Given the strength of these data with respect to numbers and completeness of follow up relative
to the preceding literature, it seems appropriate at this time strongly to consider excluding from
consideration for LVRS any subjects with a low forced expiratory volume in 1 second (FEV1)
(<20% predicted) and either low carbon monoxide transfer factor (TLCO) (<20% predicted) or
homogeneous disease. In fact, subjects with all three characteristics were at exceptionally high risk
with a 30 day mortality of 25%. This latter group often corresponds clinically to patients with
homogeneous severe destruction of alveoli and vasculature with little postoperative reserve, and
few, if any, would be likely to have suYciently mitigating characteristics that would result in an
acceptable risk.
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Sciurba
On the other hand, while it is likely that most patients having these high risk characteristics
should not be oVered surgery, ongoing analysis of NETT results may emerge which may eventually allow us to dissect the small subset of responders from non-responders within these subgroups.
Inspection of the response histograms in this paper reveals a subset of approximately 20% of all
subjects in the surgical group and none in the medical group who had a clinically substantial
response to FEV1, 6 minute walk, and maximal exercise watts. A particularly important subgroup
may be those subjects with low TLCO and heterogeneous disease. This subgroup may include
patients with extreme heterogeneity in which severely damaged lung compresses relatively
preserved lung that does not contribute to preoperative gas exchange but assumes relatively normal
mechanical and gas exchange properties postoperatively. Longer term follow up, use of quantitative CT algorithm analyses rather than qualitative scoring, and examination of the entire NETT
study population for favourable prognostic parameters such as age or exercise response may further
refine the selection. However, unless such mitigating characteristics in these high risk subgroups are
discovered, the approximately 43% chance of death per year postoperatively for only a 20% chance
of improvement seems hardly worth it.
*
ii48
c
PITFALLS IN PREDICTING RESPONSE
Brantigan’s initial experience with LVRS was thwarted in part by inadequate selection criteria
resulting in a 27% perioperative mortality rate.9 10 The team at Washington University hospital
reintroduced the open procedure with the hope that advances in physiological and radiographic
diagnostics, anaesthesia, surgical technique, and postoperative care would decrease the risks of
the procedure.11 The criteria for selection by this group included: heterogeneous emphysema with
surgical “targets”, age <75, ability to participate in a “vigorous” exercise programme, FEV1
<35% predicted, residual volume (RV) >250% predicted, and arterial carbon dioxide tension
PaCO2 <55 mm Hg (7.3 kPa).12 Using these criteria, this group reported a 90 day mortality of 4%
in a series of 150 subjects.11 While some other centres did report short term mortality rates in a
similar range,13–15 unfortunately the clinical judgement and results of these investigative teams
could not be transferred broadly despite significant exposure of the surgical community to
numerous professional lectures and on site surgical preceptorships to these centres. A report by
the US Health Care Financing Administration, which examined 711 Medicare claims for LVRS
between October 1995 and January 1996, found 3 month and 1 year mortality rates of 14.4%
and 23%.16 Apparently, there are clinical attributes targeted by experienced clinicians which have
not been overtly defined by the available selection criteria.
Different predictors for different outcomes
In LVRS we need to assess outcome using two diVerent yardsticks: (1) the incidence of morbidity
and mortality and (2) the physiological and functional response to the procedure. There is no
reason to believe that the predictors of a favourable response for each of these two outcome
dimensions will be similar. In fact, a characteristic which may be favourable for one category may
be a negative attribute to the other. An example of this phenomenon is found with the attribute
of “CT volume of emphysema” which is associated with mortality, but also correlates positively
with change in maximal exercise watts in individuals who survive to return for follow up
testing.17 18
Another factor that complicates outcome assessment in LVRS is the absence of a gold standard
of outcome for patients with chronic obstructive pulmonary disease (COPD).19 This is
particularly problematic when important outcome indices—for example, FEV1, TLCO, RV, PaO2,
exercise function, quality of life, resting and exertional dyspnoea—change disproportionately or
in opposite directions to one another. The example shown in box 1 may help to accentuate this
concept.
It would therefore not be surprising if diVerent combinations of preoperative parameters
predicted changes in the diVerent outcome indices. Finally, predictors of a short term response
may diVer from those of a long term response.
Impact of flaws in existing literature
Interestingly, many of the problems cited in the existing literature on LVRS, such as the poor
follow up rate and lack of control groups, do not have an impact on the ability to assess
predictors of short term mortality since in-hospital vital status is known in all subjects and short
term mortality in the non-surgical group is expected to be near zero (as confirmed by the NETT
high risk non-surgical group). Furthermore, determination of predictors of relative functional
outcome does not require a non-surgical control group for a meaningful analysis although
significant subject dropout and small numbers of subjects and events in the various subgroups
may impact on the validity of the analyses. By contrast, the assessment of intermediate and longer
term survival and the preoperative selection parameters that influence survival is impossible
without comparison of the LVRS group with an appropriately matched control group. The
published randomised trials are also limited in this respect either, again, because of their small
cohort size or because the nature of the crossover design prevents longer term assessment.20–22 We
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Preoperative predictors of outcome following LVRS
Box 1 Mixed outcome following LVRS
A 78 year old with diffuse, albeit mildly heterogeneous, upper
lobe disease and a TLCO of 18% predicted underwent bilateral LVRS. At 6 month follow up evaluation there were significant improvements in FEV1, RV, and resting dyspnoea
with a slight fall in TLCO but a significant decrease in exercise
tolerance and worsening of exertional hypoxaemia and dyspnoea. On examination at rest he no longer used accessory
muscles to breathe and was able to speak in full sentences
for the first time in years. However, he had developed symmetrical leg oedema and his echocardiogram indicated the
new development of RV dilation. The patient appears to have
experienced the mixed results of significant improvements in
pulmonary mechanics and lung hyperinflation with worsening
of pulmonary vascular function precipitating the development
of cor pulmonale.
-
await the longer term outcome data from NETT to provide
the initial insights into preoperative determinants which
influence long term survival for both the high risk group and
the entire cohort.
The existing literature gives conflicting results with respect
to the ability of certain preoperative variables to predict
surgical outcome. For example, previous investigators have
reported an association between low TLCO (25–30%
predicted) and surgical morbidity or mortality14 21 whereas it
was not found to be a significant determinant by others.23–25
Similarly, an arterial PCO2 value of more than 45–50 has been
implicated as an indicator of poor outcome by some,14 24 but
not by others.26 Six minute walk distances of <200 m have
been found by two groups to predict short term mortality,15 24
but not by others.23
The reasons for these conflicting results may simply be
related to the relatively small cohorts and limited numbers of
outcome events. On the other hand, overt diVerences in
exclusion criteria or unstated diVerences based on the
judgement of the surgical team may have resulted in
diVerences in characteristics of the population. For example,
a group that followed the recommendations of the early
Keenan paper by limiting the inclusion of individuals with
Table 1
low TLCO measurements may not have identified this
parameter as an independent risk factor for LVRS.
Another concern in attempting to apply selection criteria
across centres is the potential for diVerences in values based
simply on technique or the use of diVerent predicted values.
A myriad of diVerences in the technique of the 6 minute
walk test including diVerences in track length, number of
practice walks, etc can influence the final distance.27 The use
of diVerent reference values for TLCO can result in
substantial diVerences in percentage predicted measurements
reported.28 For example, the value of 20% predicted using
the Crapo normal equations, which are the reference values
used in NETT to define the high risk group, is equivalent to
a value of nearly 25% predicted using Cotes equations for a
70 year old man of height 1.6 m. Unfortunately, several
papers in the existing literature on LVRS do not even list the
reference equations or pertinent methodology used in the
determination of their reported indices.
Table 1 summarises the selection criteria identified in the
existing literature on LVRS.
Impact of surgical technique
An obvious but often overlooked variable which impacts on
outcome in individuals with otherwise similar attributes are
the subtle diVerences in surgical technique between surgeons
or centres. The amount of tissue removed and the region
selected for resection is strongly influenced by the judgement
of the surgeon. One study found a relationship between
surgical time and mortality, although specific reasons for the
increased time were not identified.23 Improved outcome
simply due to experience and a learning curve may occur
independently of baseline attributes.11 15 Another report
showed a significant relationship between the weights of
tissue removed during surgery and the degree of change in
FEV1.37 Theoretical models and animal experiments suggest
that there should be an optimal amount of lung resected to
optimise mechanics and gas exchange.38–40 Potentially even
greater determinants of final functional outcome are the
somewhat
random
occurrences
of
postoperative
complications such as pneumonia, empyema, and pulmonary
embolism. It is therefore likely that the precise prediction of
functional response based exclusively on preoperative
Preoperative predictors of outcome for LVRS
Preoperative index
Functional outcome
Physiological
TLCO
PaCO2
Morbidity outcome
– 90 day mortality 2 8 14
+ In hospital mortality14
+ Prolonged hospital stay24
+
–
–
–
RV/TLC
Raw (insp)
Raw (total)
PEEP (insp)
Shuttle walk <150 m
6 minute walk <200 m
FVC, + FEV140
FEV149
FEV129
FEV1, – dyspnoea29
– In hospital mortality2
– In hospital mortality
– Length of hospital stay15
+ Length of hospital stay
+ In hospital mortality15 23
Age >75 years
Imaging
Qualitative (segmental heterogeneity)
Qualitative (amount of compressed lung)
Qualitative (total severity)
Quantitative (upper v lower heterogeneity)
Quantitative (total % emphysema)
Quantitative (severe emphysema volume (<960
HU))
Quantitative (normal lung volume (–700 to –850))
24
+ FEV18 18 30 31
– long term FEV131
+ FEV132 34
+30 day mortality18 34
+ FEV134 35 36
+ Exercise watts17
+ PaO2, 6MW, FEV136
+ PaO2, 6MW, FEV136
TLCO=carbon monoxide transfer factor; FEV1=forced expiratory volume in 1 second; PaO2, PaCO2=arterial oxygen and
carbon dioxide tensions; RV=residual volume; PEEP=end expiratory positive pressure; +=positive association;
–=negative association.
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Sciurba
Learning points
c
*
ii50
c
c
c
c
Given the strength of the data from the NETT study with respect to numbers and
completeness of follow up relative to the earlier literature, it seems appropriate at this
time to consider excluding any subjects with a low FEV1 (<20% predicted) and either
low TLCO (<20% predicted) or homogeneous disease from consideration for LVRS
Inherent pitfalls in defining selection criteria for LVRS include: the absence of a gold
standard for outcome in COPD, potential conflicting criteria with respect to selection for
functional improvement v selection for morbidity, the uncontrollable impact of differences
in surgical technique, and postoperative complications on functional outcome
The ultimate decision on whether to perform LVRS in a given patient should depend on
a physician who is armed with accurate probabilities of outcome based on specific
preoperative patient attributes, but in the context of a discussion with that patient to
determine individual preferences
Advances in the understanding of mechanisms of response to LVRS should lead to
testable hypotheses of new selection criteria to optimise outcome
Quantitative analysis of lung CT scans is an emerging technology that should improve
consistency of radiographic indices between centres and which should continue to
evolve to optimise patient selection for LVRS
attributes will have limitations, particularly between diVerent
surgeons and institutions.
Patient preferences
Given the complexities involved with defining outcome, it
would seem that an achievable goal would be to determine
realistic probabilities of response based on a specific patient’s
attributes in order to provide more accurate informed
consent. In many respects, however, an acceptable outcome
is dependent on patients’ preferences concerning lifestyle and
their willingness to incur the risk of surgery.41 Two patients
exemplify this concept. One woman who had lived a very
active life was willing to risk a 50% chance of mortality to
have a 33% chance of playing golf again. Another, a classical
music lover and avid reader, had an acceptable lifestyle and
was not willing to risk even a 5% chance of mortality. Several
techniques have been devised to elicit patient valuations
although none has yet been reported in the LVRS
population.42 Thus, the ultimate decision on whether to
perform LVRS in a given patient should depend on a
physician who is armed with accurate probabilities of
outcome based on specific preoperative patient attributes
such as those shown in the Introductory article, but in the
context of a discussion with that patient to determine
individual preferences.
Insights into physiological mechanisms and
selection criteria
It is important to elucidate the physiological mechanisms
which lead to the changes seen following LVRS since a
greater understanding of these mechanisms should lead to
testable hypotheses with respect to new selection criteria to
optimise surgical outcome.
The improvements in lung mechanics following LVRS are
partly due to improvements in lung elastic recoil resulting in
a more rapid and complete expiratory flow that may occur in
both diVuse and heterogeneous disease.43 44 On the other
hand, regions of lung “heterogeneity” are often specifically
targeted and have such long time constants that they simply
act as space occupying residual volume. Resection of these
extremely slow lung units (in contrast to units with more
average time constants, as is likely with diVuse emphysema)
should reduce lung volume disproportionately to, and
possibly independently of, increases in global lung elastic
recoil. This concept is highlighted in a recent model
proposed by Fessler and Permutt40 which attributes the
improvements following LVRS to a more appropriate resizing
of the lung to the chest wall. In this model the dominant
impact of LVRS lies in the relatively greater reduction in
residual volume (RV) than in total lung capacity (TLC) and
a consequent increase in vital capacity (VC). This increase in
VC is the dominant factor eVecting an increase in FEV1,
which is in accordance with the relatively smaller changes in
the FEV1/FVC ratio observed in most patients following
LVRS. This model exemplifies the importance of elucidating
mechanisms, as it predicts that the best responders to LVRS
will be those with the highest preoperative RV/TLC, a
finding which has subsequently been confirmed.34 45 46
While the presence of small airway fibrosis in patients with
COPD has been known for years, its clinical significance has
been controversial.47 48 This concept has particular
significance with respect to LVRS since individuals with
disproportionate fixed small airways involvement relative to
emphysema may not experience the benefits associated with
LVRS and increased lung elastic recoil, and recent work by
Ingenito et al49 has shown a negative relationship between
preoperative inspiratory resistance and changes in FEV1
following LVRS. In a subsequent paper these authors
suggested that increased inspiratory conductance (low
inspiratory resistance) measurements assist in selecting
patients with homogeneous disease who may still respond
favourably to LVRS.45
Most of the research on LVRS has been directed at the
pulmonary mechanical eVects of the surgery. Very little
attention has been directed at its potential impact on
pulmonary vascular function, which may independently
influence exercise tolerance and survival. On the one hand,
resection of perfused lung could further decrease vascular
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Preoperative predictors of outcome following LVRS
reserve while, on the other, a decrease in vascular resistance
may occur through recruitment of vessels in re-expanding
lung tissue or through improved elastic recoil which may
increase radial traction on extra-alveolar vessels.
Furthermore, reduced end expiratory oesophageal pressure
and, hence, pericardial pressure may improve right and left
ventricular filling and cardiac output.
However, haemodynamic studies on patients before and
after LVRS show mixed results. This is not surprising given
the potentially opposing eVects described. Some reports,
including one study evaluating patients with more diVuse
disease, raise concerns about postoperative increases in
pulmonary vascular resistance both at rest and with
exertion.50 51 Conversely, a reduction in heart rate at
iso-workloads following LVRS and thus increased oxygen
pulse52 suggests that cardiovascular function improves on
average following LVRS. Also, significant increases in right
ventricular fractional area of contraction have been reported
using
echocardiographic
techniques,
suggesting
improvements in pulmonary vascular function.43 Two other
studies found no eVect on pulmonary artery pressure after
LVRS.53 54
While overall data may be mixed, it is clear from the above
studies that individual patients may experience deterioration
in pulmonary vascular function. Although definitive
preoperative identification of these individuals is not possible
at present, perhaps the preoperative power of TLCO may lie in
its ability to identify those patients at greatest risk of such
compromise.
(rind) v the central (core) lung; or quantification of
emphysema hole size.59 60 Alternatively, algorithms that define
density patterns that do not necessarily have known
subjective equivalents may have independent predictive
power.61 Ongoing advances such as comparison of thin and
thick section techniques, airway assessment, lobar isolation,
expiratory scanning, and more advanced dynamic analyses
highlight the potential of this emerging technology that
should continue to evolve to optimise patient selection for
LVRS.
Imaging analysis
References
Many studies have reported a relationship between outcome
following LVRS and the preoperative volume or pattern of
distribution of emphysema on chest computed tomographic
(CT) scanning. Unfortunately, terms describing disease
distribution such as “heterogeneous” and “homogeneous”
are not standardised and vary from centre to centre. For
example, the NETT paper8 defines heterogeneity based on
visual scoring of disproportionate disease between
non-anatomical thirds equally divided from apex to base,
whereas Weder et al30 have defined it on the basis of
disproportionate disease in consecutive anatomical segments.
Furthermore, subjective scoring has been shown to
overestimate the volume of emphysema and to exhibit poor
interobserver agreement.55
Others have used quantitative analysis programmes based
on density mask threshold values (typically –910 HU) to
categorise disease severity and pattern.56–58 Such quantitative
analysis techniques are significantly better correlated with
tissue morphometric quantification of disease (R=0.59) than
is subjective assessment (R=0.44).55 While quantitative
measures should be more acceptable as selection criteria
based on their greater ease of standardisation and more
consistent application across centres, it is not clear that
available measures provide greater discrimination of LVRS
responders and non-responders than qualitative scoring
techniques.34 Recent reports have found that varying density
mask cut oV values in order to quantitate preoperative
volume of more severe emphysema (for example, <–960 HU)
or normal lung (–700 to –850) have improved correlation
with functional outcome.36 Others have used more innovative
algorithms to assess distribution patterns. The algorithms
used to quantitate density pixel distribution patterns may
simply be designed to mimic subjective descriptions of
disease such as proportion of emphysema in the upper v
lower lung zones; proportion of disease in the peripheral
Conclusions
Data from the NETT Research Group have defined a group
of patients at high risk for LVRS. Further collection of long
term data and analysis of the entire population by the NETT
group is expected to provide further insights from this study.
Additional insights into the mechanisms of improvement and
advances in quantitative CT analysis may oVer future
advances to optimise the selection of patients for LVRS.
Acknowledgement
The author is grateful to his collaborators including Robert
Rogers, James Hogg, Harvey Coxson, William Slivka, and
Sanjay Patel for their thoughtful inspiration. While Dr
Sciurba is an investigator in NETT, the views presented are
his own and not the oYcial views of the NETT investigators.
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PREOPERATIVE PREDICTORS OF OUTCOME
FOLLOWING LUNG VOLUME REDUCTION
SURGERY
F C Sciurba
Thorax 2002 57: ii47-ii52
doi: 10.1136/thorax.57.suppl_2.ii47
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