Risk factors for morbidity after pulmonary resection for lung cancer in ...

ARTICLE IN PRESS doi:10.1510/icvts.2010.254821 Editorial

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Institutional report - Thoracic oncologic

Department of General Thoracic Surgery, Juntendo University School of Medicine, 1–3, Hongo 3-chome, Bunkyo-ku, Tokyo 113-8431, Japan b Clinical Research Center and The Center for Lifetime Cancer Education, Juntendo University School of Medicine, Tokyo, Japan

a

Abstract

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䊚 2011 Published by European Association for Cardio-Thoracic Surgery

This study retrospectively reviewed 1073 patients with NSCLCs who underwent pulmonary resection between September 1996 and October 2009 at our institute. Our surgical policy in lung cancer patients without severe co-morbidities favored lobectomy with mediastinal lymph node dissection (MLD) over limited resections, and pneumonectomy is avoided, whenever possible. Induction chemotherapy andy or radiotherapy were not routinely performed if complete resection was possible based on the radiological findings. No patient in this series received induction therapy. There were 677 males and 396 females, ranging in age from 23

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*Corresponding author. Tel.: q81-3-3813-3111; fax: q81-3-5800-0281. E-mail address: [email protected] (K. Suzuki).

2. Patients and methods

Follow-up Paper

Non-small cell lung cancer (NSCLC) is the leading cause of cancer-related death in Western countries as well as in Japan. The incidence of NSCLC diagnosed in the elderly population is rising due to the increasing life expectancy. The data of the cancer registry of Japan in 2003 showed that as many as 63.2% of lung cancers were diagnosed in patients older than 70 years of age and 24.6% in those older than 80 years of age w1x. Although surgery offers the best chance of cure for early-stage NSCLC, surgical intervention in the elderly patients has been performed with a great deal of hesitation because of the high incidence of surgical mortality and morbidity w2, 3x. The naturally shortened life expectancy and possible sequelae leading to an impaired quality of life are also additional reasons for hesitation. However, recent advances in anesthetic management, surgical techniques and perioperative management now allow for the surgical resection of NSCLC in elderly patients. In fact, many investigators reported that surgical intervention for NSCLC in the elderly is justified in terms of morbidity, mortality and residual quality of life w4–8x. Aging is associated with a significant prevalence of comorbidities w3x. Moreover, decreased reserves in various

vital organs are observed in the elderly in comparison to younger patients. Therefore, perioperative complications occurring in elderly patients, even if they are not severe, sometimes result in fatal conditions. More cautious perioperative management should therefore be conducted in elderly patients with the above distinctive characteristics in the elderly in mind. However, there have been few reports analyzing the risk factors for morbidity associated with NSCLC resection independently in younger and elderly patients w5x. The aim of this study was to evaluate the perioperative morbidity, mortality, and risk factors for morbidity after lung cancer resection in younger and elderly patients.

Negative Results

1. Introduction

Proposal for Bailout Procedure

Keywords: Lung cancer; Elderly patients; Risk factors

ESCVS Article

The aim of this study was to evaluate the perioperative morbidity, mortality, and risk factors for morbidity after lung cancer resection in younger and elderly patients. This study retrospectively reviewed 1073 patients with non-small cell lung cancers (NSCLC) who underwent pulmonary resection. The risk factors for morbidity were analyzed independently in groups of 664 younger (-70 years) patients and 409 elderly (G70 years) patients. Co-morbidities, such as hypertension, ischemic heart disease, and renal insufficiency were more frequently observed in the elderly group in comparison to the younger group. However, there were no statistical differences in the rates of overall morbidity and 30-day mortality between the younger and elderly groups (36% vs. 42% and 0.3% vs. 0.5%, respectively). Multivariate analyses revealed the risk factors for morbidity to be % forced expiratory volume in 1 s (FEV1 ), the extent of pulmonary resection and tumor histology in the younger group, and smoking, hypertension, renal insufficiency and % diffusing capacity of the lung to carbon monoxide (DLCO) in the elderly group, respectively. In conclusion, the rate of morbidity and mortality in elderly patients were similar to those observed in younger patients. However, perioperative management should be cautiously performed while taking into account the risk factors for morbidity especially in elderly patients because they frequently have various co-morbidities. 䊚 2011 Published by European Association for Cardio-Thoracic Surgery. All rights reserved.

Institutional Report

Received 3 September 2010; received in revised form 16 January 2011; accepted 26 January 2011

Protocol

Kazuya Takamochia, Shiaki Oha, Joe Matsuokab, Kenji Suzukia,*

Work in Progress Report

Risk factors for morbidity after pulmonary resection for lung cancer in younger and elderly patients

New Ideas

Interactive CardioVascular and Thoracic Surgery 12 (2011) 739–743

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to 86 years with a median age of 65 years. Fifty-two (4.8%) patients were octogenarians. Routine preoperative assessments included medical history, physical examination, basic blood tests, electrocardiogram (ECG) with exercise stress test, pulmonary function test and blood gas examination. All patients with cardiovascular disease, suspicious symptoms, or ECG abnormalities in an exercise stress test consulted a cardiologist and had additional tests, such as echocardiography and coronary angiography were performed. The diabetic status was strictly controlled under the support by diabetes specialists during the perioperative period. Clinical staging was based on a computed tomography (CT) of the chest and upper abdomen, brain CT or magnetic resonance imaging, radionuclide bone scan, andyor positron emission tomography with fluorine-18 fluorodeoxyglucose. The mediastinal and hilar lymph node status was defined as positive if the chest CT showed that the shorter axis of any node was larger than 1 cm. Mediastinoscopy and endobronchial ultrasound were not routinely performed. Morbidity was defined as any postoperative events, such as bacterial pneumonia, interstitial pneumonia, arrhythmia, prolonged air leak requiring )7 days of postoperative chest tube drainage, deliriumyconfusion, atelectasis, bleeding, chylothorax, empyema, bronchopleural fistula, or respiratory failure. The following risk factors for morbidity were evaluated independently in groups of 664 younger (-70 years) patients and 409 elderly (G70 years) patients: gender, body mass index, smoking status (pack-year), the presence of preoperative co-morbidities wdiabetes mellitus, arrhythmia, hypertension, ischemic heart disease (IHD), and liver dysfunctionx, serum creatinine (Cr) level, forced expiratory volume in 1 s (FEV1)%, %vital capacity (VC), %diffusing capacity of the lung to carbon monoxide (DLCO), past history of cancers, the extent of pulmonary resection and MLD, clinical and pathological stage, and histological cell type. Univariate analyses were performed by the x2-test. All of the variables that were found to be significant in the univariate analyses were entered into the multivariate analyses using a forward step-wise logistic regression model (0.05 for entry and 0.10 for removal probability). A P-value of -0.05 was considered to be statistically significant. All statistical analyses were performed using the SPSS statistical software package (Version 17.0, SPSS Inc, Chicago, IL, USA).

dard pulmonary resection (lobectomy or pneumonectomy, Ps0.005) and MLD (P-0.001) were more frequently performed in the younger group in comparison to the elderly group. The frequency of squamous cell carcinoma in the elderly patients was higher than in the younger patients (Ps0.006). At least one morbidity occurred in 241 (36%) of 664 younger patients and 171 (42%) of 409 elderly patients, respectively (Ps0.071). The frequency of arrhythmia (8% vs. 14%, P-0.001), prolonged air leak (6% vs. 11%, Ps0.005), and deliriumyconfusion (0.8% vs. 6%, P-0.001) after surgery were higher in the elderly group in comparison with younger group. Two patients (0.3%) in the younger group and two patients (0.5%) in the elderly group died within 30 days after surgery (Ps0.624). The causes of death were aspiration pneumonia and acute exacerbation of interstitial pneumonia in the younger group, and cerebral infarction and hemoptysis in the elderly group. The postoperative events were summarized in Table 2. Univariate analyses showed that gender, smoking status, the presence of hypertension, FEV1%, %VC, the extent of pulmonary resection and MLD, clinical stage, and histological cell type were significantly associated with morbidity in the younger group. Gender, smoking status, the presence of diabetes mellitus and hypertension, serum Cr level, FEV1%, %DLCO, and histological cell type were all found to be significant risk factors for morbidity in the elderly group (Table 3). A multivariate analysis showed that FEV1%, the extent of pulmonary resection and histological cell type remained significant risk factors for morbidity in the younger group (Table 4). Smoking status, the presence of hypertension, serum Cr level and %DLCO were significant in the elderly group (Table 5). Subgroup analyses based on the number of significant risk factors identified by the multivariate analyses were performed independently in the younger and elderly groups. The risk grade was defined as follows: low-risk: patients without any risk factors; moderate risk: patients with 1 or 2 risk factors in the younger group and patients with 1–3 risk factors in the elderly group; high-risk: patients with all risk factors. The rates of morbidity in the younger group were 7.7% (4y52) in the low-risk, 36.4% (211y579) in the moderate risk, 78.8% (26y33) in the high-risk subgroup, respectively. The rates of morbidity in the elderly group were 2.0% (1y48) in the low-risk, 46.5% (165y355) in the moderate risk, 83.3% (5y6) in the high-risk subgroup, respectively.

3. Results 4. Discussion Several clinical and pathological characteristics of patients were significantly different between the elderly and younger group (Table 1). Co-morbidities, such as hypertension (P-0.001), IHD (Ps0.002), and renal insufficiency (Ps0.001) were more frequently observed in the elderly group in comparison to the younger group. Patients with lower FEV1%, %VC and %DLCO were more common in the elderly group than in the younger group (P-0.001, Ps0.005, and P-0.001, respectively). The frequency of previous cancers other than lung cancer were higher in the elderly group than in the younger group (Ps0.001). Stan-

The present study retrospectively evaluated the risk factors for morbidity after lung cancer resection independently in younger (-70 years) and elderly (G70 years) patients. Although the definition of an elderly patient is arbitrary, a cut-off of 70 years of age was selected because the incidence of age-related physiological changes begins to increase after 70 years w9x. In addition, the incidence of overall co-morbidities in the elderly group was significantly higher than that in the younger group. Among them, hypertension, IHD, renal insufficiency, and low preoperative

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Table 1. Patient characteristics

Body mass index Smoking (pack-year) At least one co-morbidity Diabetes mellitus Arrhythmia Hypertension IHD Liver disease Cr (mgydl) FEV1% %VC %DLCO Past history of lung cancer Past history of other cancers Mode of surgery

MLD Clinical stage Pathological stage

0.34 0.23 -0.001 0.68 0.066 -0.001 0.002 0.40 0.001 -0.001 0.005 -0.001 0.92 0.001 0.005 0.065 0.010 0.045 -0.001 0.075 0.47 0.006

elderly group than the younger group in the present series. Appropriate decision-making for the surgical procedure might be one of the reasons for the equal safety and feasibility of surgical intervention in the elderly group in comparison to the younger group. Although the prevalence of both clinical and pathological early stage disease was not significantly different between

All (ns1073)

-70 years (ns664)

G70 years (ns409)

P-value

Thirty-day mortality Overall morbidities Bacterial pneumonia Interstitial pneumonia Arrhythmia Prolonged air leak Deliriumyconfusion

4 (0.4%) 412 (38%) 11 (1%) 3 (0.3%) 110 (10%) 84 (8%) 29 (3%)

2 (0.3%) 241 (36%) 5 (0.8%) 2 (0.3%) 51 (8%) 40 (6%) 5 (0.8%)

2 (0.5%) 171 (42%) 6 (1%) 1 (0.2%) 59 (14%) 44 (11%) 24 (6%)

0.62 0.071 0.26 0.86 -0.001 0.005 -0.001

Brief Case Report Communication

Event

Historical Pages

Table 2. Postoperative events

Nomenclature

pulmonary functions (lower FEV1 %, %VC and %DLCO) were more frequently observed in the elderly group in comparison to the younger group. However, there were no significant differences in terms of the rates of 30-day mortality and overall morbidities between these two groups. Kilic et al. reported segmentectomy to be associated with a decreased morbidity and mortality in elderly patients with early-stage NSCLC in comparison to lobectomy w10x. MLD was shown to be an independent risk factor for postoperative complications in octogenarians with clinical stage I NSCLC based on a review of nationwide data collected by the Japanese Joint Committee of Lung Cancer Registry w11x. Despite the higher morbidity rates of standard operative procedures, long-term survival is comparable between lobectomy and limited resection w12x and between MLD and non-MLD w13x in elderly patients with NSCLC. Limited pulmonary resection (wedge resection or segmentectomy) and omission of MLD were more frequently performed for the

Best Evidence Topic

IHD, ischemic heart disease; Cr, serum creatinine level; FEV1 , forced expiratory volume in 1 s; VC, vital capacity; DLCO, diffusing capacity of the lung to carbon monoxide; MLD, mediastinal lymph node dissection.

State-of-the-art

Histology

0.90

Follow-up Paper

259 (63%) 150 (37%) 295 (72%) 87 (21%) 224 (55%) 151 (37%) 78 (19%) 331 (81%) 355 (87%) 54 (13%) 396 (97%) 13 (3%) 265 (65%) 144 (35%) 370 (90%) 39 (10%) 396 (97%) 13 (3%) 298 (73%) 43 (11%) 137 (33%) 255 (62%) 59 (14%) 332 (81%) 205 (50%) 151 (40%) 395 (97%) 14 (3%) 338 (83%) 71 (17%) 4 (1%) 329 (80%) 35 (9%) 41 (10%) 117 (29%) 292 (71%) 280 (68%) 65 (16%) 267 (65%) 142 (35%) 274 (67%) 103 (25%) 32 (8%)

(63%) (37%) (75%) (19%) (59%) (34%) (30%) (70%) (88%) (12%) (98%) (2%) (77%) (23%) (95%) (5%) (96%) (4%) (79%) (5%) (18%) (78%) (9%) (87%) (27%) (63%) (97%) (3%) (90%) (10%) (4%) (85%) (5%) (7%) (14%) (86%) (66%) (21%) (63%) (37%) (76%) (18%) (6%)

Negative Results

418 246 500 127 391 224 200 464 582 82 654 10 512 152 633 31 636 28 525 36 117 523 60 579 177 415 642 22 595 69 26 563 31 44 95 569 437 137 419 245 504 119 41


Male Female -25 G25 F40 )40 (–) (q) (–) (q) (–) (q) (–) (q) (–) (q) (–) (q) F1.0 )1.0 -70% G70% -80% G80% -60% G60% (–) (q) (–) (q) Pneumonectomy Lobectomy Segmentectomy Wedge resection (–) (q) I II, III, IV I II, III, IV Adenocarcinoma Squamous cell carcinoma Others

ESCVS Article

Gender

P-value


G70 years (ns409)

Protocol

-70 years (ns664)


Subset

New Ideas

Variable

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Table 3. Univariate analysis of the risk factors for morbidity Variable

Younger patients (-70 years) Odds ratio (95% CI)

Gender Female Male Body mass index -25 G25 Smoking (pack-year) F40 )40 Diabetes mellitus (–) (q) Arrhythmia (–) (q) Hypertension (–) (q) IHD (–) (q) Liver dysfunction (–) (q) Cr (mgydl) F1.0 )1.0 FEV1% G70% -70% %VC G80% -80% %DLCO G60% -60% Past history of lung cancer (–) (q) Past history of other cancers (–) (q) Extent of pulmonary resection Less than lobectomy Lobectomy or more MLD (–) (q) Clinical stage II–IV I Histology Non-sq Sq

Elderly patients (G70 years) P-value

Odds ratio (95% CI)

-0.001 1.00 (reference) 1.96 (1.39–2.77)

-0.001 1.00 (reference) 2.21 (1.44–3.38)

0.97 1.00 (reference) 1.01 (0.67–1.51)

0.53 1.00 (reference) 0.85 (0.53–1.39)

-0.001 1.00 (reference) 1.89 (1.35–2.65)

-0.001 1.00 (reference) 2.18 (1.43–3.33)

0.076 1.00 (reference) 1.52 (0.96–2.43)

0.028 1.00 (reference) 1.90 (1.07–3.38)

0.81 1.00 (reference) 1.17 (0.33–4.20)

0.14 1.00 (reference) 2.29 (0.74–7.12)

0.014 1.00 (reference) 1.59 (1.10–2.29)

0.002 1.00 (reference) 1.91 (1.27–2.89)

0.29 1.00 (reference) 1.47 (0.71–3.04)

0.56 1.00 (reference) 1.22 (0.63–2.36)

0.95 1.00 (reference) 0.97 (0.44–2.15)

0.38 1.00 (reference) 1.65 (0.55–5.00)

0.27 1.00 (reference) 1.47 (0.74–2.93)

0.004 1.00 (reference) 2.61 (1.35–5.05)

-0.001 1.00 (reference) 2.46 (1.64–3.70)

-0.001 1.00 (reference) 2.05 (1.34–3.12)

0.38 1.00 (reference) 0.77 (0.44–1.37)

0.61 1.00 (reference) 1.16 (0.66–2.02)

0.022 1.00 (reference) 1.52 (1.06–2.17)

0.003 1.00 (reference) 1.94 (1.26–3.00)

0.083 1.00 (reference) 0.38 (0.13–1.14)

0.64 1.00 (reference) 0.77 (0.52–2.33)

0.11 1.00 (reference) 0.64 (0.37–1.11)

0.25 1.00 (reference) 1.35 (0.81–2.25) 0.47

-0.001 1.00 (reference) 4.77 (2.33–9.75)

1.00 (reference) 1.21 (0.72–2.01) 0.19

-0.001 1.00 (reference) 3.51 (1.98–6.25)

1.00 (reference) 1.34 (0.86–2.09) 0.006

1.00 (reference) 0.58 (0.39–0.86)

0.083 1.00 (reference) 0.62 (0.36–1.07) 0.022

-0.001 1.00 (reference) 2.05 (1.37–3.05)

P-value

1.00 (reference) 1.69 (1.08–2.65)

IHD, ischemic heart disease; Cr, serum creatinine level; FEV1 , forced expiratory volume in 1 s; VC, vital capacity; DLCO, diffusing capacity of the lung to carbon monoxide; MLD, mediastinal lymph node dissection; Sq, squamous cell carcinoma; CI, confidence interval.

the younger and elderly group, squamous cell carcinoma histology was more frequent in the elderly group than the younger group. The reasons for the difference in the histological tumor type according to the chronological age remain unclear. However, several researchers previously reported the same findings w8, 12x. Interestingly, a squamous cell carcinoma histology was a significant risk factor for morbidity according to the univariate analysis both in

the younger and elderly group, and in the younger group, it was also significant in the multivariate analysis. Several studies have found that risk factors for morbidity after pulmonary resection in elderly patients are increased age w14x, co-morbidities w4x, the extent of pulmonary resection (pneumonectomy) w15x, surgical approach (thoracotomy) w14x, and neoadjuvant therapy w5x. The current multivariate analysis found that heavy smoking history, the pre-

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Odds ratio

P-value -0.001

1.00 (reference) 2.34

1.46–3.76 -0.001


2.59–15.3 0.009


References

1.17–3.01

Variable

95% CI

P-value -0.001


1.66–4.65 0.005 1.24–3.52 0.008


1.35–6.93 0.001


1.47–4.11

Follow-up Paper State-of-the-art Best Evidence Topic Nomenclature Historical Pages

sence of hypertension, renal insufficiency and low %DLCO were significant risk factors for the elderly patients. The risk grade for morbidity based on the number of risk factors clearly stratified the patients according to the incidence of morbidity. The risk grade could be used to assist physicians and patients make decisions regarding surgery. Although chronological age is no longer a firm limitation to surgery with regard to postoperative morbidity and mortality, postoperative morbidity is well known to have a significant impact on the patients’ quality of life. Therefore, more cautious patient selection and more careful perioperative management based on the age-appropriate risk grading should be performed to make surgery an optimal intervention for NSCLC patients. The main limitation of the present study is its retrospective nature. Although our surgical policy in lung cancer patients without severe co-morbidities is lobectomy with MLD, regardless of chronological age, the final decision to perform surgical procedures may be biased based on the judgment of each primary surgeon or the wishes of the patients or their family. Although the risk factors identified in this study do not necessarily imply the true risk factors in elderly patients, we believe that such risk factors may

Negative Results

Cr, serum creatinine level; DLCO, diffusing capacity of the lung to carbon monoxide.



ESCVS Article

Smoking (pack-year) F40 )40 Hypertension (–) (q) Cr (mgydl) F1.0 )1.0 %DLCO G60% -60%

Odds ratio


Table 5. Multivariate analysis of the risk factors for morbidity in elderly patients (G70 years)

w1x Matsuda T, Marugame T, Kamo K, Katanoda K, Ajiki W, Sobue T. Cancer incidence and incidence rates in Japan in 2002: based on data from 11 population-based cancer registries. Jpn J Clin Oncol 2008;38:641–648. w2x Brown JS, Eraut D, Trask C, Davison AG. Age and the treatment of lung cancer. Thorax 1996;51:564–568. w3x Janssen-Heijnen ML, Smulders S, Lemmens VE, Smeenk FW, van Geffen HJ, Coebergh JW. Effect of comorbidity on the treatment and prognosis of elderly patients with non-small cell lung cancer. Thorax 2004;59:602– 607. w4x Birim O, Zuydendorp HM, Maat AP, Kappetein AP, Eijkemans MJ, Bogers AJ. Lung resection for non-small-cell lung cancer in patients older than 70: mortality, morbidity, and late survival compared with the general population. Ann Thorac Surg 2003;76:1796–1801. w5x Cerfolio RJ, Bryant AS. Survival and outcomes of pulmonary resection for non-small cell lung cancer in the elderly: a nested case-control study. Ann Thorac Surg 2006;82:424–429; discussion 429–430. w6x Matsuoka H, Okada M, Sakamoto T, Tsubota N. Complications and outcomes after pulmonary resection for cancer in patients 80 to 89 years of age. Eur J Cardiothorac Surg 2005;28:380–383. w7x Pagni S, McKelvey A, Riordan C, Federico JA, Ponn RB. Pulmonary resection for malignancy in the elderly: is age still a risk factor? Eur J Cardiothorac Surg 1998;14:40–44; discussion 44–45. w8x Sawada S, Komori E, Nogami N, Bessho A, Segawa Y, Shinkai T, Nakata M, Yamashita M. Advanced age is not correlated with either short-term or long-term postoperative results in lung cancer patients in good clinical condition. Chest 2005;128:1557–1563. w9x Balducci L. Geriatric oncology: challenges for the new century. Eur J Cancer 2000;36:1741–1754. w10x Kilic A, Schuchert MJ, Pettiford BL, Pennathur A, Landreneau JR, Landreneau JP, Luketich JD, Landreneau RJ. Anatomic segmentectomy for stage I non-small cell lung cancer in the elderly. Ann Thorac Surg 2009;87:1662–1666; discussion 1667–1668. w11x Okami J, Higashiyama M, Asamura H, Goya T, Koshiishi Y, Sohara Y, Eguchi K, Mori M, Nakanishi Y, Tsuchiya R, Miyaoka E. Pulmonary resection in patients aged 80 years or over with clinical stage I nonsmall cell lung cancer: prognostic factors for overall survival and risk factors for postoperative complications. J Thorac Oncol 2009;4:1247– 1253. w12x Mery CM, Pappas AN, Bueno R, Colson YL, Linden P, Sugarbaker DJ, Jaklitsch MT. Similar long-term survival of elderly patients with nonsmall cell lung cancer treated with lobectomy or wedge resection within the surveillance, epidemiology, and end results database. Chest 2005;128:237–245. w13x Okasaka T, Usami N, Taniguchi T, Kawaguchi K, Okagawa T, Suzuki H, Matsuo K, Yokoi K. Can non-performance of radical systematic mediastinal lymphadenectomy be justified in elderly lung cancer patients? An evaluation using propensity-based survival analysis. Eur J Cardiothorac Surg 2010;38:27–33. w14x Berry MF, Hanna J, Tong BC, Burfeind WR Jr, Harpole DH, D’Amico TA, Onaitis MW. Risk factors for morbidity after lobectomy for lung cancer in elderly patients. Ann Thorac Surg 2009;88:1093–1099. w15x Dyszkiewicz W, Pawlak K, Gasiorowski L. Early post-pneumonectomy complications in the elderly. Eur J Cardiothorac Surg 2000;17:246–250.

Protocol

FEV1, forced expiratory volume in 1 s; Sq, squamous cell carcinoma.


FEV1% G70% -70% Extent of pulmonary resection Less than lobectomy Lobectomy or more Histology Non-sq Sq

95% CI

New Ideas

Variable

possibly even be good candidates for use as true risk factors in these patients. In summary, the rate of perioperative morbidity and mortality after NSCLC resection in elderly patients were similar to those in younger patients. However, perioperative management should be cautiously performed while taking into account the risk factors for morbidity, especially in elderly patients because they frequently have various comorbidities.

Editorial

Table 4. Multivariate analysis of the risk factors for morbidity in younger patients (-70 years)

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Brief Case Report Communication