European Journal of Cardio-Thoracic Surgery 41 (2012) e161–e165 ORIGINAL ARTICLE

doi:10.1093/ejcts/ezs147 Advance Access publication 14 April 2012

The importance of intraoperative fluid balance for the prevention

of postoperative acute exacerbation of idiopathic pulmonary
fibrosis after pulmonary resection for primary lung cancer
Yoshimasa Mizunoa,*, Hisashi Iwataa, Koyo Shirahashia, Kazuya Takamochib, Shiaki Ohb, Kenji Suzukib
and Hirofumi Takemuraa
a
Department of General and Cardiothoracic Surgery, Graduate School of Medicine, Gifu University, Gifu, Japan
b
Division of General Thoracic Surgery, Juntendo University School of Medicine, Tokyo, Japan

* Corresponding author. Department of General and Cardiothoracic Surgery, Graduate School of Medicine, Gifu University, 1-1 Yanagido, Gifu 501-1194, Japan.
Tel: +81-58-2306325; fax: +81-58-2306326; e-mail: mizunoyoshidasa@yahoo.co.jp (Y. Mizuno).

Received 15 December 2011; received in revised form 8 February 2012; accepted 14 February 2012

Abstract
OBJECTIVES: Postoperative acute exacerbation (PAE) of idiopathic pulmonary fibrosis (IPF) is a serious complication that is hard to treat.
Therefore, it is important to manage IPF patients in such a way as to avoid PAE. Conversely, the relationship between postoperative

THORACIC
acute lung injury and perioperative fluid administration has been reported. Herein, we analyse the perioperative risk factors of PAE of
IPF, including fluid management.
METHODS: Fifty-two patients diagnosed as having clinical IPF who underwent pulmonary resection (segmentectomy, lobectomy or
bilobectomy) for primary lung cancer were analysed retrospectively. Preoperative predictive factors and perioperative management
items, especially fluid management, were evaluated.
RESULTS: The incidence of PAE of IPF was 13.5% (7 of 52 patients). Six patients (85.7%) died of respiratory failure induced by uncontrol-
lable PAE of IPF. Upon univariate analysis, the amount of the intraoperative fluid infused (ml/kg/h), the intraoperative fluid balance (ml/
kg/h) and the preoperative C-reactive protein (CRP) level were found to be significantly higher in IPF patients who developed PAE than
in those who did not. A multivariate logistic regression analysis showed that the intraoperative fluid balance and the preoperative CRP
were prognostic factors for PAE of IPF [P = 0.026, odds ratio (OR) = 1.312 and P = 0.048, OR = 1.280, respectively].
CONCLUSIONS: To prevent PAE of IPF, intraoperative management that minimizes intravenous fluid administration is essential.
Moreover, caution is particularly important in patients with preoperative evidence of inflammation.
Keywords: Idiopathic pulmonary fibrosis • Postoperative exacerbation • Primary lung cancer • Pulmonary resection • Fluid management

INTRODUCTION
Idiopathic pulmonary fibrosis (IPF) is a chronic, progressive, fi-
brotic interstitial lung disease with a median survival of 2–5
years [1]. In addition, IPF is known to be associated with primary
lung cancer. It has been reported that the incidence of primary
lung cancer is increased in patients with IPF, ranging from 7.5 to
17.8%, and the effect is independent of the effect of cigarette
smoking [2, 3]. Postoperative acute exacerbation (PAE) of IPF is
associated with a high mortality rate after pulmonary resection;
of all the postoperative complications, it is the most likely to be
fatal [4–7]. Although some authors have attempted to identify
the predictors and the appropriate perioperative management
for the prevention of PAE of IPF [4–8], none have been
established.
Conversely, fluid management is reported to be an important
factor for acute lung injury (ALI) after thoracic surgery [9–11].
Therefore, we hypothesized that perioperative fluid balance was
an important factor related to PAE of IPF, and reviewed the post-
operative results of IPF patients with primary lung cancer at two
institutions.
PATIENTS AND METHODS
From July 2004 to March 2011, the data of 1444 consecutive
patients with primary lung cancer who underwent pulmonary
resection at two institutions, Gifu University and Juntendo
University School of Medicine, were retrospectively analysed. Of
the 1444 patients, 62 (4.3%) had IPF clinically, and 52 of the 62
patients who underwent pulmonary resection excluding pneu-
monectomy and pulmonary wedge resection were assessed. The
patients were diagnosed as having clinical IPF with American
Thoracic Society (ATS)/European Respiratory Society (ERS) cri-
teria for the diagnosis of IPF in the absence of a surgical lung
biopsy [12]. This study was approved by the Gifu University and

© The Author 2012. Published by Oxford University Press on behalf of the European Association for Cardio-Thoracic Surgery. All rights reserved.
e162 Y. Mizuno et al. / European Journal of Cardio-Thoracic Surgery
Juntendo University Institutional Review Boards for Clinical
Research.
Preoperative evaluation, including a complete history, physical
examination and laboratory findings (including arterial blood gas
analysis, chest roentgenogram, electrocardiogram, pulmonary
function tests and computed tomography (CT) of the chest and
abdomen), was performed in all patients. Selected patients
underwent an 18F-fluorodeoxyglucose positron emission tomog-
raphy, bronchoscopy, brain magnetic resonance imaging, echo-
cardiogram, myocardial perfusion scintigraphy or coronary
angiography for further assessment.
Before surgery, a thoracic epidural catheter was inserted rou-
tinely. After anaesthesia induction, patients were intubated using
a double-lumen endotracheal tube for one-lung ventilation. The
fraction of inspired oxygen during surgery was minimized by the
anaesthesiologist, based on the intraoperative arterial blood gas
analysis. In order to enter the thorax, a posterolateral or antero-
lateral thoracotomy with thoracoscopic assistance through a 7 to
25 cm long skin incision was performed. A hilar and mediastinal
lymph node dissection was performed based on the progression
of the lesion. In general, patients were extubated at the end of
the operation and transferred to the intensive care unit or ward.
A prophylactic medication to prevent PAE of IPF was adminis-
tered depending on the patient’s condition and the decision of
the doctor in charge. Chest radiographs were routinely taken on
every postoperative day (POD). A chest CT was not performed
routinely. Additional chest radiographs and CT were taken for
further evaluation depending on the patient’s clinical course
rather than for all abnormal symptoms and signs. If infiltration
was seen on the chest radiograph and CT, patients were diag-
nosed as having PAE of IPF, based on the following criteria [13]:
(i) aggravation of dyspnoea; (ii) hypoxaemia with an arterial
oxygen tension/inspired oxygen tension ratio of <225; (iii) newly
developing pulmonary infiltrates on chest radiography and (iv)
the absence of apparent infection or heart disease. Especially,
the differential diagnosis between PAE of IPF and postoperative
infection is important. Upon the occurrence of the abnormal
shadow on a chest X-ray and CT, we performed the tests for the
infectious diseases, e.g. white blood cell count, C-reactive
protein (CRP), procalcitonin, D-beta-glucan, Aspergillus antigen,
Candida antigen, cytomegalovirus pp65 antigenaemia,
Pneumocystis carinii DNA, sputum culture and blood culture. We
consulted respiratory physicians and radiologists about the clin-
ical and radiographic diagnosis. Moreover, we administered
broad-spectrum antibiotics. Under the consideration of the
results of the tests and reaction of antibiotics, we denied post-
operative infection.
The inhalation dosage of postoperative oxygen was minimized
to maintain SpO2 at 92% or greater, and to maintain the patient’s
physical condition.
When PAE of IPF developed, a steroid pulse therapy with
methylprednisolone was given as the first-line treatment. If the
steroid pulse therapy was not effective, a second-line treatment
was given, which included an immunosuppressive drug and/or
a polymyxin B-immobilized fibre column haemoperfusion
treatment.
We assessed all resected specimens regardless of whether the
patients had usual interstitial pneumonia (UIP), with histological
findings. In this series, we excluded the patients diagnosed as
having other diffuse parenchymal lung diseases, e.g. emphysema,
chronic obstructive lung disease, non-specific interstitial
pneumonia, bronchitis and sarcoidosis. However, if the resected
specimens did not include the area of fibrosis or honeycombing,
especially the tumour located in the upper lobe, they could not
provide the confidential pathological findings for UIP/IPF.
Therefore, we included the patients who could be diagnosed as
having clinical IPF, according to the ATS/ERS criteria.
For comparisons between the two groups, PAE of IPF(−) and
PAE of IPF(+), statistical evaluation was performed using IBM
SPSS Statistics 18 software (SPSS, Chicago, IL, USA). Differences
in categorical values were tested by χ 2 test (or Fisher’s exact
test). Continuous values were tested by an unpaired Student’s
t-test. A Mann–Whitney U-test was used to compare non-
normally distributed data. A multivariate analysis was performed
using a logistic regression test. All the values with P < 0.10 at the
univariate analysis were entered in a multivariate analysis. P <
0.05 was considered as significant.
RESULTS
Of the 52 patients, seven (13.5%) developed PAE of IPF, which
occurred from the 2nd to the 13th day (median, 6th day) after
surgery. The mortality rate of PAE of IPF was 85.7%; all deaths
were caused by severe respiratory failure induced by uncontrol-
lable PAE of IPF. Only one patient recovered in response to the
steroid pulse therapy.
As detailed in Table 1, the patient characteristics of the two
groups were similar; there were no significant differences, except
for the preoperative CRP levels. Similarly, there were no signifi-
cant differences in the arterial blood gas and pulmonary func-
tion test values, including percentage diffusion capacity for
carbon monoxide (DLCO), between the two groups. Five kinds
of prophylactic medications (nafamostat mesilate, hydrocorti-
sone, sivelestat sodium hydrate, sivelestat sodium hydrate +
methylprednisolone and methylprednisolone) to prevent PAE of
IPF were given. No significant difference in these medical treat-
ments was seen between the groups.
The intraoperative and postoperative findings are listed in
Table 2. Upon univariate analysis, the amount of intraoperative
fluid infused (7.71 ± 3.11 versus 10.3 ± 3.66 ml/kg/h, P = 0.049)
and the intraoperative fluid balance (4.99 ± 2.86 versus 8.00 ±
4.21 ml/kg/h, P = 0.035) were significantly greater in patients
who developed PAE of IPF than in those who did not. Body
weight change, defined as the maximum body weight gain from
the preoperative day to the discharge day or the onset day of
PAE of IPF, and body weight change up to POD 1, defined as the
body weight change from the preoperative day to POD 1, were
not significantly different between the two groups. There were
also no significant differences in the oncological factors (tumour
size, histology, tumour location and pathological stage) or in the
occurrence of postoperative complications. Regarding the post-
operative complications, prolonged air leak, mild pneumonia (all
cases were cured with antibiotics), chylothorax, gastric ulcer,
atrial fibrillation, the elevation of transaminase and aggravation
of the chronic rheumatoid arthritis symptom were shown.
As shown in Table 3, the multivariate logistic regression ana-
lysis showed that intraoperative fluid balance and CRP were the
predictive factors for the postoperative PAE of IPF [P = 0.026,
odds ratio (OR) = 1.312 and P = 0.048, OR = 1.280, respectively].
 Y. Mizuno et al. / European Journal of Cardio-Thoracic Surgery e163

Table 1: Preoperative patient characteristics and clinical data—the univariate analysis

PAE of IPF(−) PAE of IPF(+) P-value

Age (years) 72.1 ± 7.54 68.6 ± 8.48 0.277

Sex (male/female) 43/2 7/0 0.747
Preoperative corticoid medication (+/−) 41/4 5/2 0.180
Prophylactic medication (none/nafamostate 21/2/1/7/11/3 1/1/0/1/4/0 0.170
mesilate/hydrocortisone/sivelestat sodium
hydrate/sivelestat sodium hydrate +
methylpredonisolone/methylpredonisolone)
DLCO (%) 51.4 ± 21.1 48.9 ± 14.3 0.899
VC (%) 96.3 ± 16.7 87.8 ± 10.5 0.200
VC (ml) 3110 ± 500 2910 ± 576 0.341
FEV1.0 (ml) 2200 ± 359 2180 ± 324 0.897
FEV1.0 (%) 74.2 ± 11.6 81.7 ± 9.56 0.110
TV (ml) 728 ± 282 764 ± 264 0.668
PaO2 (mmHg) 81.7 ± 10.4 79.5 ± 13.1 0.625
PaCO2 (mmHg) 41.1 ± 4.10 37.8 ± 5.99 0.074
KL-6 (U/ml) 652 ± 480 530 ± 241 0.689
Smoking (pack year) 57.5 ± 32.3 51.0 ± 27.8 0.742
WBC (/μl) 6490 ± 2230 8170 ± 2440 0.061
CRP (mg/dl) 0.85 ± 1.9 3.4 ± 5.3 0.021
LDH (IU/l) 225 ± 66.6 189 ± 48.1 0.096
CEA (ng/ml) 10.1 ± 19.0 6.93 ± 6.77 0.862

THORACIC
DLCO: diffusion capacity for carbon monoxide; WBC: white blood cell count; CRP: C-reactive protein; LDH: lactate dehydrogenase; CEA: carcinoembryonic
antigen; VC: vital capacity.

Table 2: Intraoperative and postoperative data, including oncological findings—the univariate analysis

PAE of IPF(−) PAE of IPF(+) P-value

Operative procedure (S/L/BL) 5/38/2 0/6/1 0.192

Operation time (min) 220 ± 110 230 ± 79.1 0.601
Anaesthesia time (min) 304 ± 132 348 ± 100 0.203
Blood loss (ml) 117 ± 128 186 ± 148 0.140
Amount of intraoperative fluid infused (ml/kg/h) 7.71 ± 3.11 10.3 ± 3.66 0.049
Intraoperative fluid balance (ml/kg/h) 4.99 ± 2.86 8.00 ± 4.21 0.035
Body weight change (kg) 1.06 ± 1.22 1.93 ± 1.68 0.120
Body weight change until 1POD (kg) 0.16 ± 1.3 1.3 ± 1.6 0.122
Duration of chest drainage (days) 5.7 ± 7.5 5.1 ± 3.1 0.661
Tumour size (mm) 36.5 ± 16.1 38.5 ± 15.3 0.714
Histology (ad/sq/others) 17/19/9 3/3/1 0.729
Tumour location (RUL/RML/RLL/LUL/LLL) 7/2/21/1/14 1/1/2/0/3 0.775
Pathological stage (IA/IB/IIA/IIB/IIIA/IIIB) 8/10/8/5/10/4 2/2/0/0/2/1 0.816
Postoperative complications (+/−) 15/30 4/3 0.221

S: segmentectomy; L: lobectomy; BL: bilobectomy; POD: postoperative day; Ad: adenocarcinoma; sq: squamous cell carcinoma; RUL: right upper lobe;
RML: right middle lobe; RLL: right lower lobe; LUL: left upper lobe; LLL: left lower lobe.

DISCUSSION
Table 3: Predictive factors of PAE of IPF on multivariate
analysis As a result of recent advances in preoperative evaluation, surgi-
cal techniques, anaesthesia and postoperative care, the mortality
OR (95% CI) P-value after surgery for lung cancer has been kept very low (30-day
mortality, 0.4%) in Japan [14]. In this report, of the 237 deaths
Intraoperative fluid balance 1.312 (1.034–1.667) 0.026
CRP 1.280 (1.003–1.635) 0.048
after pulmonary resection for lung cancer, 63 were caused by
PAE of IPF [14]. Therefore, IPF is one of the most important risk
PAE of IPF: postoperative exacerbation of idiopathic pulmonary
factors for morbidity and mortality after pulmonary resection.
fibrosis; CI: confidence interval; CRP: C-reactive protein. Currently, surgery has been established as the primary treatment
for lung cancer. Even in patients with IPF, the long-term efficacy
e164 Y. Mizuno et al. / European Journal of Cardio-Thoracic Surgery
of surgical treatment for lung cancer has been reported [5, 15,
16]. In the cases of chemotherapy and radiation therapy for lung
cancer with IPF, the incidence of treatment-related PAE of IPF
was reported to range from 5.6 to 21% [17] and around 25%[18],
respectively. Conversely, the incidence of surgery-related PAE of
IPF was reported to range from 7.1 to 20% [4–7]; therefore,
surgery cannot be avoided without a thought, if there is radical-
ity for lung cancer. However, because of the high mortality rate
(75–100%) of PAE of IPF when it occurs [4–7], it is important to
prevent PAE of IPF. Some authors have reported the predictive
factors for the development of PAE of IPF. Exertional dyspnoea,
CRP, lactate dehydrogenase (LDH), restrictive ventilatory impair-
ment, percent DLCO, tumour histology and KL-6 have been
reported as predictive factors [4, 6, 7]. In the present study,
patient characteristics, pulmonary function test results, onco-
logical characteristics and laboratory findings other than CRP did
not show any significant differences between the patients who
did and did not develop PAE of IPF. Some reports [4, 5, 8] sug-
gested that the incidence of PAE of IPF correlated with the
extent of the pulmonary resection. The results of the present
study showed that patients with larger pulmonary resections
(lobectomy and bilobectomy) had a higher incidence of post-
operative exacerbations, albeit non-significantly. The one patient
who underwent pneumonectomy and the nine who underwent
wedge resections were excluded from this study. Some authors
reported a high incidence of postoperative ALI occuring in
patients who underwent pneumonectomy [11]. Because pneu-
monectomy itself is considered to be a risk factor, we excluded
the patient with pneumonectomy. Conversely, the patients who
underwent wedge resections were excluded because we consid-
ered that wedge resections had less influence on intrapulmonary
circulation for the following reasons: (i) The pulmonary vascular
bed hardly decreases. (ii) There is no injury of the lymphatic
systems. Regarding the intraoperative blood loss, although statis-
tical significance was not detected, the amount of blood loss
tended to be more in patients who developed PAE of IPF. The
blood loss and consequently the required higher intraoperative
fluid administration, together, could support at least an adverse
tendency of PAE of IPF.
On the other hand, since excessive fluid infusion has been
reported to be one of the risk factors for ALI after thoracic
surgery for lung cancer [9, 10], we analysed fluid management to
determine whether it could be a risk factor for PAE of IPF. Licker
et al. [9] identified fluid infusion during anaesthesia as one of the
risk factors for the development of primary ALI after lung resec-
tion. The patients who did and did not develop ALI received 9.1
and 7.2 ml/kg/h of intraoperative fluid infusion, respectively [9].
In the present study, patients who did and did not develop PAE
of IPF received 10.3 and 7.71 ml/kg/h fluid infused, respectively.
Thus, 7–8 ml/kg/h is considered as the proper amount of intrao-
perative fluid infusion for patients undergoing pulmonary resec-
tion. Moreover, because intraoperative fluid balance is more
important, as revealed in the present study, it is desirable that it
be restricted to within 5 ml/kg/h, considering urinary excretion
and blood loss. With respect to water balance during surgery,
Okamoto et al. [6] reported no significant difference between
patients who did and did not develop PAE of IPF. Because they
compared the two groups simply on the basis of water balance
(ml), a different result could have been obtained had they ana-
lysed the value corrected for the patient’s weight and operation
time. With respect to the assessment of postoperative fluid man-
agement, weight gain from the preoperative state was analysed
in the present study. Because the patients usually had meals
from POD 1, fluid balance could not be assessed using the
amount of fluid infused. Though changes in body weight both
throughout the clinical course and up to POD 1 showed no sig-
nificant differences between the two groups, the patients who
developed PAE of IPF tended to gain weight postoperatively.
With respect to the prophylactic medication to prevent PAE of
IPF, there is no definitive evidence. Even corticosteroid therapy,
which has been analysed most frequently, has been controversial
[13, 16]. In the present study, there was no significant difference
among the five kinds of regimens used. To establish the most
appropriate prophylactic treatment, prospective, controlled trials
are required.
In the present study, a thoracotomy was performed with thor-
acoscopic assistance and a 7 to 25 cm long skin incision to ap-
proach the lung. Koizumi et al. [4] and Akiba et al. [19] described
the effectiveness of the video-assisted thoracic surgery approach.
However, compared with our data, operation time and blood
loss were greater in both reports [4, 6]. Despite there being no
significant difference between the two groups in terms of oper-
ation time and blood loss, we consider that a short operation
time and low blood loss are preferable, and we adopted a pos-
terolateral or anterolateral thoracotomy with thoracoscopic as-
sistance and a minimal skin incision as the appropriate
approach.
STUDY LIMITATIONS
A retrospective analysis is susceptible to various factors of bias,
which could not have been identified and controlled. In the
present study, we could not analyse the data of ventilatory man-
agement of one-lung ventilation. We recognize that the values
of a fraction of inhalation oxygen (FiO2) and tidal volume (TV),
which were reported as the predictors of post-thoracotomy ALI
[20], may be important factors for PAE of IPF. Therefore, we
managed the FiO2 and TV as low as possible to maintain SpO2
>90% during operation. Because the value of FiO2 and TV were
various, we could not collect suitable data.
Another limitation is that we could not present the haemo-
dynamic parameters. Diaper et al. [21] reported the benefit of
transoesophageal Doppler monitoring (TDM) during the intrao-
perative period for restrictive fluid strategy for undergoing lung
cancer resection. To decide the favourable amount of fluid infu-
sion during the intraoperative and postoperative period, further
examination is needed. The haemodynamic parameters shown
by intraoperative TDM or postoperative transthoracic echocar-
diogram are considered to be helpful for a detailed analysis.
Because of the small sample size of this study, we may have
indicated an accidental relationship between the amount of
intraoperative fluid infused and PAE of IPF. Therefore, a rando-
mized control study that minimizes the patient bias, including
the preoperative prophylactic medication and the intraoperative
value of a FiO2, TV, one-lung ventilation time, lateral position
time and other hidden factors, is needed.
CONCLUSIONS
This study is the first to demonstrate the importance of fluid
management for the prevention of PAE of IPF. Although further
study is needed, intraoperative fluid infusion should be minimized
 Y. Mizuno et al. / European Journal of Cardio-Thoracic Surgery
for patients, especially those with IPF and an inflammatory reac-
tion before surgery, who undergo pulmonary resection.
Conflict of interest: none declared
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