Risk assessment of lung resection for lung cancer ...

Risk assessment of lung resection for lung cancer according to pulmonary function: republication of systematic review and proposals by guideline committee of the Japanese Association for Chest Surgery 2014 Noriyoshi Sawabata, Takashi Nagayasu, Yoshihisa Kadota, Taichiro Goto, Hiroyoshi Horio, et al. General Thoracic and Cardiovascular Surgery ISSN 1863-6705 Gen Thorac Cardiovasc Surg DOI 10.1007/s11748-014-0475-x

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Author's personal copy Gen Thorac Cardiovasc Surg DOI 10.1007/s11748-014-0475-x

CURRENT TOPICS REVIEW ARTICLE

Risk assessment of lung resection for lung cancer according to pulmonary function: republication of systematic review and proposals by guideline committee of the Japanese Association for Chest Surgery 2014 Noriyoshi Sawabata • Takashi Nagayasu • Yoshihisa Kadota Taichiro Goto • Hiroyoshi Horio • Takeshi Mori • Shinichi Yamashita • Akinori Iwasaki

•

Received: 10 July 2014 Ó The Japanese Association for Thoracic Surgery 2014

Abstract Background This manuscript provides preoperative physiologic assessments for patients considered for surgical resection of lung cancer. Methods Medical studies of risk assessment of surgical resection for lung cancer according to pulmonary function were collected and a review article was written to present guidelines. Results Preoperative physiologic assessment should begin with a cardiovascular evaluation, and spirometry to measure FEV 1 and the diffusing capacity of carbon monoxide (DLCo). Predicted postoperative (ppo) lung functions should also be calculated. If both %ppo-FEV 1 and %ppo-DLCo values are C60 %, the patient is This review was submitted at the invitation of the editorial committee. This article is based on a study first reported at the online site of the Japanese Association of Chest Surgery (http://www.jacsurg.gr.jp/). For the Japanese Association of Chest Surgery. N. Sawabata (&) Department of General Thoracic Surgery, Hoshigaoka Medical Center, Hirakata, Japan e-mail: [email protected] T. Nagayasu Division of Surgical Oncology, Department of Surgery, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, Japan Y. Kadota Department of Thoracic Surgery, Osaka Prefectural Medical Center for Respiratory and Allergic Disease, Habikino, Japan

considered to be at low risk for anatomic lung resection. If either of those are \60 % of the predicted value, an exercise test should be performed for screening. If performance on the exercise test is acceptable, the patient is regarded to be at low risk for anatomic resection. These findings can be summarized as an algorithm. Conclusions Careful preoperative physiologic assessment is useful for identifying patients at increased risk for standard lung cancer resection and enabling informed decisions by the patient about an appropriate therapeutic approach for their lung cancer. Keywords Lung cancer Pulmonary resection Cardiopulmonary function Risk assessment

Introduction It is quite difficult to assess the risk of surgery for lung cancer, as various aspects must be considered such as H. Horio Department of Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital, Tokyo, Japan T. Mori Department of Thoracic surgery, Kumamoto University School of Medicine, Kumamoto, Japan S. Yamashita A. Iwasaki Department of Thoracic, Endocrine and Pediatric Surgery, Faculty of Medicine, Fukuoka University, Fukuoka, Japan

T. Goto Department of Surgery, Yamanashi Prefectural Central Hospital, Yamanashi, Japan

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Author's personal copy Gen Thorac Cardiovasc Surg

perioperative complications, perioperative death, and longterm cardiopulmonary function, as well as others. Although surgery is generally the best curative option for patients with early-stage non-small cell lung cancer, many potentially resectable tumors occur in individuals with impaired pulmonary function, who may be at increased risk for both immediate perioperative complications and long-term disability following curative-intent surgical resection. This study was performed to provide guidelines for preoperative physiologic assessment of patients being considered for surgical resection of lung cancer.

Mortality rates during the perioperative period have been shown to be reduced in certified hospitals staffed by certified surgeons [21–23], thus surgery for lung cancer should be carried out in such institutions. In addition, though a previous study found that the time period between time of diagnosis and surgery does not influence prognosis [24], the operation should be performed as soon as possible. Also, induction chemotherapy has an influence on preoperative pulmonary function, especially DLCo, resulting in an increased rate of postoperative complications [25].

Materials and methods

Risk assessment of mortality and morbidity in perioperative period

One of the authors (N.S.) reviewed manuscripts regarding risk assessment of lung resection for lung cancer according to pulmonary function and wrote a review article to present guidelines, which was reviewed by members of the guideline committee of the Japanese Association of Chest Surgery. Furthermore, public comments were called for at the online site of the Japanese Association of Chest Surgery (http://www.jacsurg.gr.jp/). Thereafter, the final version of the article was completed.

The rate of complications or death in lung cancer patients during the perioperative period has been decreasing [13– 17]. Furthermore, with developments in anesthesia and operation techniques, the rate of cardiopulmonary complications, such as acute hypercapnia, mechanical ventilation over 48 h, arrhythmia, pneumonia, and atelectasis, requiring a bronchoscopy has decreased, whereas the rate of postoperative atrial fibrillation remains high [1, 12, 17]. Assessment of cardiovascular condition

Results General remarks The physiological background of patients considered as candidates for lung surgery contributes to the risk of surgery, with cardiopulmonary background being the most important factor [1, 2]. When cardiovascular risk is suspected, preoperative risk assessment is mandated [3]. In addition, age seems to influence perioperative risk, though rarely disturbs curative treatment [5–11], as preoperative complications seem to be most important to predict postoperative death [1, 4]. According to the guidelines of the American College of Chest Physicians, the risk of death due to the operation is approximately 5 % in lobectomy and 10 % in pneumonectomy cases [1, 12]. However, in reports from the Japanese Joint Committee of Lung Cancer Registry, the rate of perioperative death including hospital death in all surgical cases was 3.1 % in 1994 [13, 17], 2.0 % in 1999 [14, 16], and 0.8 % in 2004 [17]. In addition, the rate of death within 30 days after surgery in Japan was reported to be 0.4 % in 2004 [17]. Furthermore, patients greater than 80 years old have a similar risk of perioperative mortality as compared to younger patients, ranging from 0 to 3 % in Japanese reports [5–11, 13–18], and 2 to 16 % in reports presented in Europe and the United States [19, 20].

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In surgery for lung cancer, risk assessment of cardiovascular condition is mandated even in cases of limited surgery, because there are many patients with smoking and/or arteriosclerosis as comorbid factors. The American Heart Association presented guidelines for assessment of noncardiovascular surgery that utilize multiple steps [26] and perioperative cardiovascular risk (myocardial infarction, heart failure, cardiac death) in lung cancer patients should be determined using those, as follows. First step: Determine whether non-cardiovascular surgery is urgent. If yes, surgery should be done. Second step: In cases of non-urgent surgery, the first priority is assessment of active cardiac issue: (1) unstable angina, (2) decompensated cardiac failure, (3) significant arrhythmia, and (4) severe vulvar disease, which should be treated as a priority. Third step: In cases with non-active cardiovascular disease, selection should be carried out according to the grade of surgery risk, as an operation is generally performed for low risk patients. However, since surgery for pulmonary disease is categorized as moderate risk, the next step is necessary. Fourth step: In cases with stable cardiovascular disease and surgery risk that is moderate or greater, an operation is performed when the patient has an exercise capacity greater than four metabolic equivalent (MET). In general, MET [10 is excellent, 7–10 is good, 4–6 is moderate, and


\4 is poor. MET4 in Japan is referred to as the capability to make a bed, clean a room, walk 6 km in 1 h, play one round of golf using a cart, go bowling, play catch with a baseball, and other similar activities. Fifth step: In cases with dyspnea on effort or exercise capacity \MET4, surgery is performed if there are no clinical risk factors. However, in those with at least one factor, further examinations and assessments are necessary. Those risk factors can vary, for example ischemic heart disease, decompensation heart failure or history of that, diabetes mellitus, renal function disorder, and brain vessel disorder [26]. Assessment of respiratory function Pulmonary function test (spirometry) The most common test for assessment of risk of chest surgery is forced expiratory volume 1 (FEV1). In addition, a pulmonary function test should be done when the candidate is in stable condition or receiving appropriate medication. Thresholds for postoperative mortality less than 5 % are FEV1 [1.5 L in lobectomy cases and [2.0 L in pneumonectomy cases [27–31]. Although the risk of surgery for lung cancer may be underestimated when using an absolute value in aged, small body, and female patients, in cases with %FEV1 [80 % there is a low risk of perioperative mortality including pneumonectomy candidates [32]. In addition, postoperative predictive FEV1 (ppoFEV1) most precisely predicts postoperative pulmonary function. In general, that is determined using lung perfusion scintigraphy and the formula for ppo-FEV1 is as follows. Ppo-FEV1 = preoperative FEV1 9 (residual segment number/total segment number). This method is easy and efficacious in lobectomy cases. A previous report stated that the total number of lung segments is 18 (right upper lobe: 3, right middle lobe: 2, right lower lobe: 5, left upper lobe 4, right lower lobe: 4) [27]. However, in Japan, it is common to consider that the left upper lobe has five segments, because its volume is greater than the other pulmonary lobes. Although some studies used a more detailed technique, that formula has a high correlation (r = 0.87–0.96) [33]. Perioperative mortality risks according to FEV1 are summarized in Table 1 [34–43]. A number of clinical investigations have shown that the risk of perioperative mortality is increased from 30 to 50 % in cases with ppoPEV \40 %. On the other hand, there are few studies that assessed ppo-FEV1 for operative mortality in cases of sublobar resection, though one report noted that a segmentectomy was allowed for surgical resection in patients with stage I NSCLC and impaired respiratory reserve

without compromising oncological results, but with preservation of respiratory function [44]. Gas exchange capacity Although normal arterial blood gas examination results seem to be important for perioperative assessment of pulmonary resection cases, some studies that examined this issue found that moderate hypercapnia does not influence perioperative mortality or morbidity [35, 36, 45–47]. In addition, a study that assessed PaO2 revealed that there was no significant difference in perioperative mortality between groups with PaO2 greater and lower than 60 mmHg (6 vs. 7 %) [36]. Thus, a pulmonary resection should be determined not only by arterial blood gas results, but also by an integrated assessment that includes volume of the resected pulmonary parenchyma and exercise capacity, as well as others [37]. Diffusing capacity of lung for carbon monoxide: DLCo DLCo measurement is also effective for perioperative risk assessment of pulmonary resection, and perioperative mortality risk assessed according to %DLCo and %ppoDLCo is summarized in Table 2 [38, 41, 42, 48–51]. The rate of perioperative mortality increases in patients with %DLCo \60 % and increases with decreasing %ppoDLCo. Furthermore, the rate of perioperative morbidity has been shown to be increased in patients with %DLCo \80 %, thus surgery in those patients should be carefully performed. Exercise function capacity An exercise capacity test can evaluate whole body functions including cardiopulmonary function, thus the feasibility of pulmonary resection in light of physical stress is more accurately assessed with it as compared to other tests. During exercise, O2 consumption and CO2 exudate cause cardiac output to increase to adjust the O2 supply, which uses all of the heart, lungs, and related vessels. With heavy exercise stress, oxygen consumption reaches a horizontal plateau, which is the maximum oxygen consumption (VO2max). Assessments of perioperative mortality risk using VO2max are summarized in Table 3 [35, 38, 41, 42, 51–53]. In cases of standard surgery, the rate of perioperative mortality increases in cases with VO2max \20 mL/kg/min, though factors other than VO2max should be considered for operability. In addition, the rate of perioperative mortality is greater than 25 % in cases with VO2max \10 mL/kg/min [38, 42, 52, 54]. There are some simple methods available to measure exercise capacity, such as maximum walking distance or

123

123

1992

1992

1989

Holden et al. [42]

Nakagawa et al. [43]

Markos et al. [38]

ppo-FEV1.0

ppo-FEV1.0

ppo-FEV1.0

ppo-FEV1.0

ppo-FEV1.0

ppo-FEV1.0

pre-FEV1.0 pre-FEV1.0

pre-FEV1.0

pre-FEV1.0

Few All Few Few

\40 % \40 %

Few

\1 L

\40 %

Few

\1 L

\40 %

Few Few

\60 % \60 %

Few

Few

\1.3 L

Few

Few

\1.5 La

\40 %

All

\1.5 La

\40 %

High risk patients (%)

Threshold

0

0

31

26

0

0

0

20

11 18

20

18

15

77

77

44

54

77

0

62

52

74 56

52

56

70

23

23

25

20

23

100

38

28

15 26

28

26

15

b

a

Any complications

\2 L for pneumonectomy

41

24

6

41

157

122

38

542

43 69

562

71

11

NA

12

21

17

(78)

16 b

0

8

0

10

NA

3

0

7

(32)b 13

NA 3

6

(33)b 21 10

1

NA

Perioperative death (%)

8

27

Pulmonary complication (%)

N

Pneumonectomy

Wedge

Lobectomy

High risk patients

Pulmonary resection (%)

FEV1 forced expiratory volume in 1 s, pre preoperative, ppo predicted postoperative, NA not assessed

1994

Pierce et al. [41]

ppo-FEV1.0

1989

Markos et al. [38]

1989

1997

Duque et al. [36]

1985

1993 1995

Dales et al. [37] Bolliger et al. [35]

Wahi et al. [39]

1997

Duque et al. [36]

Nakahara et al. [40]

ppo-FEV1.0

1995

Bolliger et al. [35]

pre-FEV1.0

1989

Olsen et al. [34]

Test

Year

References

Table 1 Perioperative mortality risk according to FEV1

6

7

10

13

15

51

9

63

50 11

30

9

18

N

50

71

60

(85)

47

NA

33

b

(37)b

50 100

(27)b

44

22


50

29

50

38

NA

16

33

6

NA 9

13

22

NA


Moderate risk patients


pre-DLCo

ppo-DLCo

ppo-DLCo

ppo-DLCo

1994

1989

1995

1992

1989

1994

1995

Pierce et al. [41]

Markos et al. [38]


Holden et al. [42]

Markos et al. [38]

Pierce et al. [41]

Ferguson et al. [49]

pre-DLCo

All Few Few Few

\50 % \40 % \40 % \40 %

Few All

\50 %

Few

\60 % \50 %

Few Few

\60 % \60 %


Threshold

0

0

26

0

31

0

0

26

0

75

75

54

62

44

46

62

54

69

25

25

20

38

25

54

38

20

31

1987

1989

Bechard et al. [52]

Markos et al. [38]

a

NA not assessed Any complications

1984

Smith et al. [53]

1989

Markos et al. [38]

1992

1995


1994

1995


Price [41]

1987

Bechard et al. [52]

Holden et al. [42]

Year

References

VO2max

VO2max

VO2max

NO2max

VO2max

VO2max

VO2max

VO2max

VO2max

Test


Many Few All Few All Few Few Many Few

Threshold

\15 \15 \15 \15 \15 \15 \15 \10 \10

Table 3 Perioperative mortality risk according to VO2max

a

262

0

24

27

26

31

0

0

18

24

62

56

55

54

44

62

59

56

56

38

20

18

20

25

38

41

26

20

38

43

16

44

NA

29

NA

64

28

16

18

7

18

0

6

NA

3

NA

1

0

NA 19

2–13


(77)a

14

NA

6

7


N

Pneumonectomy

Wedge

8–33

17

(77)a

38 3

High risk patients

Lobectomy

0 0

10

50

14

6

17

(770)a

5 5

10

?

7

14

8

11

14

7

20

62

N

34

(71)a

67

38

27

43

(71)a

45

18


5

7

6

8

11

14

17

16

22

N

0

71

83

(88)a

36

21

29

38

40


0

29

17

25

27

7

18

13

13


22

43

33

25

27

21

14

25

5





19


?

47

32

8

14

32

47

145


N

Pneumonectomy

Wedge

Lobectomy

High risk patients


DLCO carbon monoxide diffusing capacity of lung, pre preoperative, ppo predicted postoperative Any complications

pre-DLCo

pre-DLCo

ppo-DLCo

pre-DLCo

1996

1988

Bousamara et al. [50]

Test

Ferguson et al. [48]

Year

References

Table 2 Perioperative mortality risk according to DLCo

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Gen Thorac Cardiovasc Surg

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stair climbing. However, though utilized in clinical practice, those are difficult to standardize and few studies have used them to evaluate perioperative mortality. Maximum walking distance is measured using a shuttle walk test or 6-min walking test (6MWT). For the shuttle walk test, the patient is asked to walk between two points 10 m apart according to signal pacing. If 25 shuttles cannot be performed, exercise capacity may be VO2max \10 mL/kg/min [55, 56], though 6MWT has also not

been standardized [57]. Generally, VO2max is [15 mL/kg/ min in individuals who are able to climb more than three floors (54 steps, 18.5 cm each) and \10 ml/kg/min in those who can climb less than one floor (18 steps) [58]. In addition, an individual who can climb a sufficient number of steps but is affected by comorbidities also has a high risk of perioperative mortality [59–62], as the threshold for a lobectomy is three stairs and that for a pneumonectomy is five stairs.

Fig. 1 Algorithm for risk assessment of patients scheduled for pulmonary resection. FEV forced expiratory volume, ppo predicted postoperative, DLCO diffusing capacity or transfer factor of lung for carbon monoxide

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Desaturation Walking test findings can indicate patients with desaturation more easily than an exercise capacity test. Although the clinical implications are obscure, the risks of perioperative morbidity and mortality are high in cases with desaturation [4 % [27, 38, 41, 63].

2. 3.

4.

Algorithm for risk assessment of patients scheduled for pulmonary resection

5.

According to the present results, an algorithm for risk assessment of patients scheduled for pulmonary resection was constructed (Fig. 1) and no public comments critical of it have been presented.

6.

7.

8.

Discussion Based on findings presented in this review, %FEV1, %DLCo, ppo%FEV1, and ppo%DLCo, as well as exercise capacity test results are recommended for assessment of perioperative risk in patients undergoing a pulmonary resection. In detail, predicted postoperative (ppo) lung functions should be calculated as follows. If both %ppoFEV 1 and %ppo-DLCo values are C60 %, the patient is considered to be at low risk of anatomic lung resection. If either is \60 % of the predicted value, an exercise test should be performed as a screening examination. If performance on the exercise test is acceptable, the patient is regarded to be at low risk for an anatomic resection. These findings can be summarized as an algorithm for such risk assessment, as shown in Fig. 1.

9. 10.

11. 12.

13.

14. 15.

Conclusions

16.

Careful preoperative physiologic assessments are useful for identifying patients at increased risk when undergoing standard lung cancer resection and enable them to make an informed decision regarding the appropriate therapeutic approach for treating their lung cancer.

17.

Acknowledgments We thank the former members of the guideline committee of the Japanese Association of Chest Surgery and all who provided public comments. Conflict of interest declare.

None of the authors have competing interests to

18.

19.

20.

References 21. 1. Brunelli A, Kim AW, Berger KI, Addrizzo-Harris DJ. Physiologic evaluation of the patient with lung cancer being considered

for resectional surgery: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidencebased clinical practice guidelines. Chest. 2013;143:e166S–90S. Miyoshi S. Preoperative evaluation of cardiopulmonary function in patients with lung cancer. JJLC. 2003;43:675–85. Hood RM. Preoperative management. In: Techniques in general thoracic surgery. Philadelphia: W.B. Saunders Company; 1985. p. 1–12. Expert Advisory Group. A policy framework for commission cancer services. London: Department of Health; 1955. Dominguez-Ventura A, Allen MS, Cassivi SD, Nichols FC 3rd, Deschamps C, Pairolero PC. Lung cancer in octogenarians: factors affecting morbidity and mortality after pulmonary resection. Ann Thorac Surg. 2006;82:1175–9. Osaki T, Shirakusa T, Kodate M, Nakanishi R, Mitsudomi T, Ueda H. Surgical treatment of lung cancer in octogenarian. Ann Thorac Surg. 1994;57:188–93. Matsuoka H, Okada M, Sakamoto T, Tsubota N. Complication and outcomes after pulmonary resection for cancer in patients 80 to 89 years of age. Eur J Cardiothorac Surg. 2005;28:380–3. Naunheim KS, Kesler KA, D’Orazio SA, Fiore AC, Judd DR. Lung cancer surgery in the octogenarian Eur J Cardiothorac Surg. 1994;8:453–6. Pagni S, Federico JA, Ponn RB. Pulmonary resection for lung cancer in octogenarians. Ann Thorac Surg. 1997;63:785–9. Brock MV, Kim MP, Hooker CM, et al. Pulmonary resection in octogenarians with stage I nonsmall cell lung cancer: a 22-year experience. Ann Thorac Surg. 2004;77:271–7. Port JL, Kent M, Korst RJ, et al. Surgical resection for lung cancer in the octogenarian. Chest. 2004;126:733–8. Colice GL, Shaferd S, Griffin JP, Keenan R, Bolliger CT. Physiologic evaluation of the patient with lung cancer being considered for resectional surgery: aCCP evidence based clinical practice guidelines. Chest. 2007;132:161–77. Shirakusa T, Kobayashi K. Lung Cancer in Japan: analysis of lung cancer registry for resected cases in 1994. JJLC. 2002;42:555–66. Shimokata K, Sohara Y. Lung cancer in Japan: analysis of lung cancer registry for resected cases in 1999. JJLC. 2007;47:299–311. Goya T, Asamura H, Yoshimura H, Kato H, Shimokata K, Tsuchiya R, Sohara Y, Miya T, Miyaoka E. Japanese Joint Committee of lung cancer registry. Prognosis of 6644 resected nonsmall cell lung cancers in Japan: a Japanese lung cancer registry study. Lung Cancer. 2005;50:227–34. Asamura H, Goya T, Koshiishi Y, Sohara Y, Eguchi K, Mori M, Nakanishi Y, Tsuchiya R, Shimokata K, Inoue H, Nukiwa T, Miyaoka E. Japanese Joint Committee of lung cancer registry. A Japanese lung cancer registry study: prognosis of 13,010 resected lung cancers. J Thorac Oncol. 2008;3:46–52. Sawabata N, Asamura H, Goya T, Mori M, Nakanishi Y, Eguchi K, Koshiishi Y, Okumura M, Miyaoka E, Fujii Y. Japanese Joint Committee for lung cancer registry. Japanese lung cancer registry study of 11,663 surgical cases in 2004: demographic and prognosis changes over decade. J Thorac Oncol. 2011;6:1229–35. Sakata Y, Fujii Y, Kuwano H. Thoracic and Cardiovascular surgery in Japan during 2008. Gen Thorac Cardiovasc Surg. 2010;58:356–83. Goodney PP, Lucas FL, Stukel TA, et al. Surgeon specialty and operative mortality with lung resection. Ann Surg. 2005;241:179–84. Romano PS, Mark DH. Patient and hospital characteristics related to in-hospital mortality after lung cancer resection. Chest. 1992;101:1332–7. Bach PB, Cramer LD, Schrag D, et al. The influence of hospital volume on survival after resection for lung cancer. N Engl J Med. 2001;345:181–8.

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Author's personal copy Gen Thorac Cardiovasc Surg 22. Birkmeyer JD, Siewers AE, Finlayson EVA, et al. Hospital volume and surgical mortality in the United States. N Engl J Med. 2002;346:1128–37. 23. Birkmeyer JD, Stukel TA, Siewers AE, et al. Surgeon volume and operative mortality in the United States. N Engl J Med. 2003;349:2117–27. 24. Aragoneses FG, Moreno N, Leon P, et al. Influence of delays on survival in the treatment of bronchogenic carcinoma. Lung Cancer. 2002;36:59–63. 25. Matsubara Y, Takeda S, Mashimo T. Risk stratification for lung cancer surgery. Chest. 2005;128:3519–25. 26. Fleisher LA, Beckman JA, Brown KA, et al. ACC/AHA 2007 guideline on perioperative cardiovascular evaluation for noncardiac surgery. Circulation. 2007;1116:e418–500. 27. British Thoracic Society. Society of Cardiothoracic Surgeons of Great Britain and Ireland Working Party. Guidelines on the selection of patients with lung cancer for surgery. Thorax. 2001;56:89–108. 28. Boushy SF, Billig DM, North LB, et al. Clinical course related to preoperative and postoperative pulmonary function in patients with bronchogenic carcinoma. Chest. 1971;59:383–91. 29. Wernly JA, DeMeester TR, Kirchner PT, et al. Clinical value of quantitative ventilation-perfusion lung scans in the surgical management of bronchogenic carcinoma. J Thorac Cardiovasc Surg. 1980;80:535–43. 30. Miller JI Jr. Physiologic evaluation of pulmonary function in the candidate for lung resection. J Thorac Cardiovasc Surg. 1993;105:347–51. 31. Ali MK, Mountain CF, Ewer MS, et al. Predicting loss of pulmonary function after resection for bronchogenic carcinoma. Chest. 1980;77:337–42. 32. Wyser C, Stulz P, Soler M, et al. Prospective evaluation of an algorithm for the functional assessment of lung resection candidates. Am J Respir Crit Care Med. 1999;159:1450–6. 33. Zeiher B, GrossTJ Kern JA, et al. Predicting postoperative pulmonary function in patients undergoing lung resection. Chest. 1995;108:68–72. 34. Olsen GN, Weiman DS, Bolton JW. Submaximal invasive exercise testing and quantitative lung scanning in the tolerance for lung resection. Chest. 1989;101:1369–75. 35. Bolliger CT, Jordan P, Soler M. Exercise capacity as a predictor of postoperative complications in lung resection candidates. Am J Respir Crit Care Med. 1995;151:1472–80. 36. Duque JL, Ramos G, Gastrodeza J, et al. Early complications in surgical treatment of lung cancer: a prospective, multicenter study. Ann Thorac Surg. 1997;63:944–50. 37. Dales RE, Dionne G, Leech JA, et al. Preoperative prediction of pulmonary complications following thoracic surgery. Chest. 1993;104:155–9. 38. Markos J, Mullan BP, Hillan DR, et al. Preoperative assessment as a predictor of mortality and morbidity after lung resection. Am Rev Respir Dis. 1989;139:902–10. 39. Wahi R, McMutery MJ, DeCaro LF, et al. Determination of perioperative morbidity and mortality after pneumonectomy. Ann Thorac Surg. 1989;48:33–7. 40. Nakahara K, Monden Y, Ohno K, et al. A method for predicting postoperative lung function and its relation to postoperative complications in patients with lung cancer. Ann Thorac Surg. 1985;39:260–5. 41. Price R, Copland JM, Sharpe K. Preoperative risk evaluation for lung cancer resection: predicted postoperative product as a predictor of surgical mortality. Am J Respir Crit Care Med. 1994;150:947–55. 42. Holden DA, Rice TW, Stelmach K, et al. Exercise testing, 6-min walk, and stair climb in the evaluation of patients at high risk for pulmonary resection. Chest. 1992;102:1774–9.

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43. Nakagawa K, Nakahara K, Miyoshi S, et al. Oxgen transport during incremental exercise load as a predictor of operative risk in lung cancer patients. Chest. 1992;101:1369–75. 44. Martin-Ucar AE, Nakas A, Pilling JE, West KJ, Waller DA. A case-matched study of anatomical segmentectomy versus lobectomy for stage I lung cancer in high-risk patients. Eur J Cardiothorac Surg. 2005;27:675–9. 45. Kearney DJ, Lee TH, Reilly JJ, et al. Assessment of operative risk in patients undergoing lung resection: importance of predicted pulmonary function. Chest. 1994;150:947–55. 46. Walsh GL, Morice RC, Putnam JB, et al. Resection of lung cancer is justified in high-risk patients selected by exercise oxygen consumption. Ann Thorac Surg. 1994;61:1494–500. 47. Bolliger CT, Soler M, Stulz P. Evaluation of high-risk lung resection candidates: pulmonary hemodynamics versus exercise testing. Respiration. 1994;61:181–6. 48. Ferguson MK, Little L, Rizzo L, et al. Diffusing capacity predicts morbidity and mortality after pulmonary resection. J Thoracic Cardiovasc Surg. 1988;96:894–900. 49. Ferguson MK, Reeder LB, Mick R. Optimizing selection pf patients for major lung resection. J Thoracic Cardiovasc Surg. 1995;109:275–83. 50. Bousamra M, Presberg KW, Chammas JH, et al. Early and late morbidity in patients undergoing pulmonary resection with low diffusion capacity. Ann Thorac Surg. 1996;62:968–75. 51. Bolliger CT, Wyser C, Roser H, et al. Lung scanning and exercise testing for the prediction of postoperative performance in lung resection candidates at increased risk for complications. Chest. 1995;108:341–8. 52. Bechard D, Wetstein L. Assessment of exercise oxygen consumption as preoperative criterion for lung resection. Ann Thorac Surg. 1987;44:344–9. 53. Smith TP, Kinasewiz GT, Tucker WY, et al. Exercise capacity as a predictor of post-thoracotomy morbidity. Am Rev Respir Dis. 1984;129:730–4. 54. Olsen GN, Weiman DS, Bolton JWR, et al. Submaximal invasive exercise testing and quantitative lung scanning in the evaluation for tolerance of lung resection. Chest. 1989;95:267–73. 55. Singh SJ, Morgan MD, Scott S, et al. Development of a shuttle walking test of disability in patients with chronic airway obstruction. Thorax. 1992;47:1019–24. 56. Win T, Jackson A, Groves AM, et al. Relationship of shuttle walk test and lung cancer surgical outcome. Eur J Cardiothorac Surg. 2004;26:1216–9. 57. Turner SE, Eastwood PE, Cecins NM, et al. Physiologic responses to incremental and self-paced exercise in COPD. Chest. 2004;126:766–73. 58. Pollock M, Roa J, Benditt J, et al. Estimation of ventilator reserve by stair climbing. Chest. 1993;104:1378–83. 59. Brunelli A, Sabbatini A, Xiume F, et al. Inability to perform maximal stair climbing test before lung resection. Eur J Cardiothorac Surg. 2005;27:367–72. 60. Brunelli A, Monteverde M, Refai MA, et al. Stair climbing test as a predictor of cardiopulmonary complications after pulmonary lobectomy in the elderly. Ann Thorac Surg. 2004;77:266–70. 61. Smith TP, Kinasewiz GT, Tucker WY, et al. Exercise capacity as a predictor of post-thoracotomy morbidity. Am Rev Respir Dis. 1984;129:730–4. 62. Cerfolio RJ, Allen MS, Trastek VF, et al. Lung resection in patients with compromised pulmonary function. Ann Thorac Surg. 1996;62:348–51. 63. Ninan M, Summers KE, Landreneau RJ, et al. Standardised exercise oximetry predicts postpneumonectomy outcome. Ann Thorac Surg. 1997;64:328–33.