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Aging and disease    2015, Vol. 6 Issue (6) : 466-477     DOI: 10.14336/AD.2015.0503
Original Article |
Influence of Pulmonary Rehabilitation on Lung Function Changes After the Lung Resection for Primary Lung Cancer in Patients with Chronic Obstructive Pulmonary Disease
Mujovic Natasa1,2,*(), Mujovic Nebojsa2,3, Subotic Dragan2,4, Ercegovac Maja2,4, Milovanovic Andjela1,2, Nikcevic Ljubica5, Zugic Vladimir2,6, Nikolic Dejan2,7
1Clinic for Physical Medicine and Rehabilitation, Clinical Center of Serbia, Belgrade, Serbia
2Faculty of Medicine, University of Belgrade, Belgrade, Serbia
3Clinic for Cardiology, Clinical Center of Serbia, Belgrade, Serbia
4Clinic for Thoracic Surgery, Clinical Center of Serbia, Belgrade, Serbia
5Special Hospital for Cerebrovascular Disorders “Saint Sava“, Belgrade, Serbia
6Clinic for Pulmonary disease and TB, Clinical Center of Serbia, Belgrade, Serbia
7Department of Physical Medicine and Rehabilitation, University Children’s Hospital, Belgrade, Serbia
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Influence of physiotherapy on the outcome of the lung resection is still controversial. Study aim was to assess the influence of physiotherapy program on postoperative lung function and effort tolerance in lung cancer patients with chronic obstructive pulmonary disease (COPD) that are undergoing lobectomy or pneumonectomy. The prospective study included 56 COPD patients who underwent lung resection for primary non small-cell lung cancer after previous physiotherapy (Group A) and 47 COPD patients (Group B) without physiotherapy before lung cancer surgery. In Group A, lung function and effort tolerance on admission were compared with the same parameters after preoperative physiotherapy. Both groups were compared in relation to lung function, effort tolerance and symptoms change after resection. In patients with tumors requiring a lobectomy, after preoperative physiotherapy, a highly significant increase in FEV1, VC, FEF50 and FEF25 of 20%, 17%, 18% and 16% respectively was registered with respect to baseline values. After physiotherapy, a significant improvement in 6-minute walking distance was achieved. After lung resection, the significant loss of FEV1 and VC occurred, together with significant worsening of the small airways function, effort tolerance and symptomatic status. After the surgery, a clear tendency existed towards smaller FEV1 loss in patients with moderate to severe, when compared to patients with mild baseline lung function impairment. A better FEV1 improvement was associated with more significant loss in FEV1. Physiotherapy represents an important part of preoperative and postoperative treatment in COPD patients undergoing a lung resection for primary lung cancer.

Keywords pulmonary rehabilitation      preoperative physiotherapy      lung cancer      lobectomy      pneumonectomy     
Corresponding Authors: Mujovic Natasa     E-mail:
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present address: Kunming Biomed International, Kunming, Yunnan, 650500, China

Issue Date: 01 December 2015
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Mujovic Natasa
Mujovic Nebojsa
Subotic Dragan
Ercegovac Maja
Milovanovic Andjela
Nikcevic Ljubica
Zugic Vladimir
Nikolic Dejan
Cite this article:   
Mujovic Natasa,Mujovic Nebojsa,Subotic Dragan, et al. Influence of Pulmonary Rehabilitation on Lung Function Changes After the Lung Resection for Primary Lung Cancer in Patients with Chronic Obstructive Pulmonary Disease[J]. Aging and disease, 2015, 6(6): 466-477.
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Group A (n=56)Group B (n=47)p
Age (years) MV±SD62±759±90.134
Male gender N (%)49(88)41(87)0.968
Smoking history N (%)50(89)44 (94)0.438
Co-morbidities N (%)50(89)34(72)0.027
Hypertension N (%)28(50)18(38)0.234
Coronary disease N (%)11(20)9(19)0.950
Heart failure N (%)4(7)1(2)0.238
Diabetes mellitus N (%)7(13)4(8)0.514
Chronic renal failure N (%)0(0)2(4)0.119
COPD stage: I/II/III/IV N (%)10(18)/ 39(69)/ 6(11)/ 1(2)24(51)/ 22(47)/ 1(2)/ 0(0)0.002
Basal spirometry:
FEV1 (mL) MV±SD1948±5692509±741<0.001
FEV1% pred. MV±SD65±1479±18<0.001
VC (mL) MV±SD3352±8733731±10880.055
VC% pred. MV±SD88±1594±210.116
Tiffneau index % MV±SD56±862±6<0.001
FEF50% MV±SD29±1444±24<0.001
IC% MV±SD74±1184±12<0.01
FEF25% MV±SD27±1842±240.001
Pulmonary resection:
Pneumonectomy N (%)13(23)5(11)0.094
Lobectomy N (%)43(77)42(89)0.094
Total hospital stay (days) MV±SD36±1925±12<0.001 stay (days) MV±SD21±129±6<0.001 stay (days) MV±SD16±916±80.571
Total complications N (%)20(36)21(45)0.354
Pulmonary complications N (%)17(30)20(43)0.199
In-hospital mortality N (%)2(4)0(0)0.191
Table 1  Baseline patients characteristics
Figure 1.  Changes in FEV1 parameter. (A) Correlation between the gain in FEV1 and prolongation of the 6MWD during the preoperative physiotherapy. (B) Inverse correlation between the amplitude of FEV1 improvement after preoperative physiotherapy and postoperative loss in FEV1. FEV1=forced expiratory volume in the first second, in liters; 6MWD=six minute walking distance, in meters; Pre-PR=preoperative pulmonary rehabilitation.
n = 43Before Pre-PR (T1)after Pre-PR (T2)after resection (T3)Δ [T2-T1]Δ [T2-T3]Δ [T1-T3]
mean [95% CI]mean changemean [95% CI]mean changemean [95% CI]mean change
FEV1 (ml)1985±5442334±6201795±544346** [ 259, 434]20%566** [ 470, 661]23%189* [ 77, 300]7%
FEV1 % pred.64±1476±1558±1311** [ 9, 13]20%19** [ 15, 22]23%6** [ 3, 10]7%
VC (ml)3394±8413877±8783068±858469** [369, 569]17%763** [590, 935]20%284* [93, 475]6%
VC % pred.89±16103±1681±1513** [ 11, 16]18%22** [ 18, 26]21%8** [3, 12]6%
Tiffeneau index (%)55±959±955±103** [ 1, 5]7%5** [ 2, 7]7%1* [-2, 4]1%
IC (%)75±1184±777±9-*9%-*7%-2%
FEF50 (%)30±1534±1419±113** [1, 6]18%12** [8, 16]39%10** [5, 14]29%
FEF25 (%)30±1632±1619±122* [-1, 5]16%11** [ 7, 16]36%11** [5, 16]25%
6MWD (m)375±99428±91349±9153** [42, 64]16%85** [71, 100]19%31** [18, 44]6%
Dyspnea before 6MWT2.2±0.91.2±0.82.0±0.6-1.0** [-0.8, -1.2]--0.8** [-0.5, -1.1]-0.2 [-0.2, 0.6]-
Dyspnea after 6MWT3.2±0.92.1±0.82.9±0.7-1.1** [-0.9, -1.3]--1.0** [-0.7, -1.3]-0.2 [-0.2, 0.6]-
Table 2  Changes of the lung function, effort tolerance and symptomatic status in patients of the Group Awith lobectomy
n=13before Pre-PR (T1)after Pre-PR (T2)after resection (T3)Δ [T2-T1]Δ [T2-T3]Δ [T1-T3]
mean [95% CI]% changemean [95% CI]% changemean [95% CI]% change
FEV1 (ml)1888±6252127±5011344±392236 [45, 426]17824** [640, 1009]38576** [390, 763]29
FEV1 % pred.65±1274±1248±69* [3, 16]1628** [22, 35]3618** [13, 24]27
VC (ml)3216±9273565±8312187±672296 [17, 574]131385** [1071, 1700]391105** [820, 1391]33
VC % pred.89±1699±1862±1010 [1, 18]1338** [29, 47]3729** [23, 35]31
Tiffeneau index (%)58±660±857±123 [0, 7]44 [-2, 10]70 [-8, 7]1
IC (%)73±1382±1470±11-*9-**12-3
FEF50 (%)30±1033±818±113 [-1, 7]1515** [6, 24]4412* [1, 23]32
FEF25 (%)31±932±1117±111 [-6, 9]1215* [5, 26]3813* [3, 23]39
6MWD (m)354±78422±82327±7455** [34, 76]2187** [66, 108]2331** [16, 46]8
Dyspnea before 6MWT2.5±0.91.4±0.92.1±0.5-1.0** [-0.7, -1.3]--0.9* [-0.3, -1.5]-0 [-0.7, 0.7]-
Dyspnea after 6MWT3.5±0.92.4±0.63.3±0.6-1.0** [-0.7, -1.3]--1.0** [-0.5, -1.5]-0 [-0.7, 0.7]-
Table 3  Changes of the lung function, effort tolerance and symptomatic status in patients of the Group A with pneumonectomy
Figure 2.  Changes of lung function parameters before and after resection. (A) Change in FEV1 (mL) before and after resection in the Group A and Group B, [*] p<0.001. (B) Change in VC (mL) before and after resection in the Group A and Group B, [*] p=0.055. (C) Change in FEF50 (black line) and FEF25 (gray line) before and after resection in the Group A and Group B, [*, #] p<0.001, [†, ‡, §] p<0.05. (D) Change in 6MWD (in meters) before and after lung resection in the Group A and Group B, [*] p<0.05. FEV1=forced expiratory volume in the first second; VC=vital capacity; 6MWD=six minute walking distance; FEF50/25=forced expiratory flow; T1=values at admission to hospital; T2=values before resection (after physiotherapy); T3=values after surgery. Filled line and dotted line represent Group A and Group B, respectively.
Figure 3.  Changes in IC% before and after lung resection. Group A (full line) and Group B (dotted line), * p<0.05 Group A T1 vs Group B T1, # p<0.05 Group A Δ(T1-T2). T1=values at admission to hospital; T2=values before resection (after physiotherapy); T3=values after surgery.
FEV1<50% mean [95% CI] (n=7)50%≤FEV1<80% mean [95% CI] (n=39)FEV1≥80% mean [95% CI] (n=10)p-value
Δ[T2-T1]FEV1 (mL)427 [27, 827]328 [242, 414]235 [74, 396]0.631
FEV1 % pred.40 [-4, 86]18 [14, 22]9 [3, 16]0.107
FEF50 (%)7 [-14, 27]3 [0, 6]3 [1,6]0.857
FEF25 (%)2 [-21, 24]4 [1, 7]-4 [-15, 6]0.220
Δ[T2- T3]FEV1 (mL)442 [180, 703]580 [491, 667]749 [511, 987]0.152
FEV1 % pred.25 [14, 36]26 [22, 30]27 [19, 34]0.980
FEF50 (%)9 [3, 16]11 [7, 15]*22 [16, 28]*0.004
FEF25 (%)6 [2, 11]9 [5, 14]†21 [12, 31]†0.039
Table 4  Postoperative lung function changes depending on severity of COPD at admission in the Group A.
[1] Brunelli A, Charloux A, Bolliger CT, Rocco G, Sculier JP, Varela G, Licker M, Ferguson MK, Faivre-Finn C, Huber RM, Clini EM, Win T, De Ruysscher D, Goldman L; European Respiratory Society and European Society of Thoracic Surgeons joint task force on fitness for radical therapy (2009). ERS-ESTS clinical guidelines for evaluating fitness for radical treatment (surgery and chemoradiotherapy) in patients with lung cancer. Eur Respir J, 34:17-41.
[2] Ohno Y, Koyama H, Takenaka D, Nogami M, Kotani Y, Nishimura Y, Yoshimura M, Yoshikawa T, Sugimura K (2007). Coregistered ventilation and perfusion SPECT using krypton-81m and Tc-99m-labeled macroaggregated albumin with multislice CT utility for prediction of postoperative lung function in non-small cell lung cancer patients. Acad Radiol, 14:830-8.
[3] Yoshimoto K, Nomori H, Mori T, Kobayashi H, Ohba Y, Shibata H, Shiraishi S, Kobayashi T (2009). Prediction of pulmonary function after lung lobectomy by subsegments counting, computed tomography, single photon emission computed tomography and computed tomography: a comparative study. Eur J Cardiothorac Surg, 35:408-13.
[4] Sullivan V, Tran T, Holmstrom A, Kuskowski M, Koh P, Rubins JB, Kelly RF (2005).Advanced age does not exclude lobectomy for non-small cell lung carcinoma. Chest, 128:2671-6.
[5] Sawada S, Komori E, Nogami N, Bessho A, Segawa Y, Shinkai T, Nakata M, Yamashita M (2005). Advanced age is not correlated with either short-term or long-term postoperative results in lung cancer patients in good clinical condition. Chest, 128:1557-63.
[6] Wang JS, Abboud RT, Evans KG, Finley RJ, Graham BL (2000). Role of CO diffusing capacity during exercise in the preoperative evaluation for lung resection. Am J Respir Crit Care Med, 162:1435-44.
[7] Mujovic N, Mujovic N, Subotic D, Marinkovic M, Milovanovic A, Stojsic J, Zugic V, Grajic M, Nikolic D (2014).Preoperative Pulmonary Rehabilitation in Patients with Non-small Cell Lung Cancer and Chronic Obstructive Pulmonary Disease. Arch Med Sci, 10:68-75.
[8] Pauwels RA, Buist AS, Calverley PM, Jenkina CR, Hurd SS, GOLD Scientific Committee (2001). Global strategy for diagnosis, management and prevention of chronic obstructive pulmonary disease. NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) workshops summary. Am J Respir Crit Care Med, 163:1256-76.
[9] Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CP, Gustafsson P, Jensen R, Johnson DC, MacIntyre N, McKay R, Navajas D, Pedersen OF, Pellegrino R, Viegi G, Wanger J; ATS/ERS Tas Force (2005). Standardisation of spirometry. Eur Respir J, 26: 319-38.
[10] Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault J-C (1993). Lung volume and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European RespiratorySociety. Eur Respir J Suppl, 16:5-40.
[11] De Leyn P, Lardinois D, Van Schil PE, Rami-Porta R, Passlick B, Zielinski M, Waller DA, Lerut T, Weder W (2007). ESTS guidelines for preoperative lymph node staging for non-small cell lung cancer. Eur J Cardiothorac Surg, 32:1-8.
[12] ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories (2002). ATS statement: Guidelines for the Six-Minute Walk Test. Am J Respir Crit Care Med, 166: 111-7.
[13] Mador MJ, Rodis A, Magalang UJ (1995). Reproductibility of Borg scale measurements of dyspnea during exercise in patients with COPD. Chest, 107;1590-7.
[14] Cesario A, Ferri L, Galetta D, Cardaci V, Biscione G, Pasqua F, Piraino A, Bonassi S, Russo P, Sterzi S, Margaritora S, Granone P (2007). Pre-operative pulmonary rehabilitation and surgery for lung cancer. Lung Cancer, 57:118-9.
[15] Weiner P, Man A, Weiner M, Rabner M, Waizman J, Magadle R, Zamir D, Greiff Y (1997).The effect of incentive spirometry and inspiratory muscle training on pulmonary function after lung resection. J Thorac Cardiovasc Surg, 113:552-7.
[16] Ozalevli S, Ilgin D, Karaali HK, Bulac S, Akkoclu A (2010). The effect of in-patient chest physiotherapy in lung cancer patients. Support Care Cancer, 18:351-8.
[17] Bobbio A, Chetta A, Ampollini L, Primomo GL, Internullo E, Carbognani P, Rusca M, Olivieri D (2008). Preoperative pulmonary rehabilitation in patients undergoing lung resection for non-small cell lung cancer. Eur J Cardiothorac Surg, 33:95-8.
[18] Jones LW, Peddle CJ, Eves ND, Haykowsky MJ, Courneya KS, Mackey JR, Joy AA, Kumar V, Winton TW, Reiman T (2007). Effects of presurgical exercise training on cardiorespiratory fitness among patients undergoing thoracic surgery for malignant lung lesions. Cancer, 110:590-8.
[19] Liu W, Pan YL, Gao CX, Shang Z, Ning LJ, Liu X (2013). Breathing exercises improve post-operative pulmonary function and quality of life in patients with lung cancer: A meta-analysis. Exp Ther Med, 5:1194-200.
[20] Divisi D, Di Francesco C, Di Leonardo G, Crisci R (2013). Preoperative pulmonary rehabilitation in patients with lung cancer and chronic obstructive pulmonary disease. Eur J Cardiothorac Surg, 43:293-6.
[21] Pehlivan E, Turna A, Gurses A, Gurses HN (2011). The effects of preoperative short-term intense physical therapy in lung cancer patients: a randomized controlled trial. Ann Thorac Cardiovasc Surg, 17:461-8.
[22] British Thoracic Society; Society of Cardiothoracic Surgeons of Great Britain and Ireland Working Party (2001). BTS guidelines: guidelines on the selection of patients with lung cancer for surgery. Thorax, 56:89-108.
[23] Colice GL, Shafazand S, Griffin JP, Keenan R, Bolliger CT; American College of Chest Physicians (2007). Physiologic evaluation of the patient with lung cancer being considered for resectional surgery: ACCP evidenced-based clinical practice guidelines (2nd edition). Chest, 132(Suppl 3):161S-177S.
[24] Korst RJ, Ginsberg RJ, Ailawadi M, Bains MS, Downey RJ Jr, Rusch VW, Stover D (1998).Lobectomy improves ventilatory function in selected patients with severe COPD. Ann Thorac Surg, 66:898-902.
[25] Subotić D, Mandarić D, Eminović T, Gajic MM, Mujovic NM, Atanasijadis ND, Dzeletovic PP, Andric LD, Bulajic BM, Dimitrijevic ID, Sobic DP (2007).Influence of chronic obstructive pulmonary disease on postoperative lung function and complications in patients undergoing operations for primary non-small cell lung cancer. J Thorac Cardiovasc Surg, 134:1293-8.
[26] Baldi S, Ruffini E, Harari S, Roviaro GC, Nosotti M, Bellaviti N, Venuta F, Diso D, Rea F, Schiraldi C, Durigato A, Pavanello M, Carretta A, Zannini P (2005).Does lobectomy for lung cancer in patients with chronic obstructive pulmonary disease affect lung function? A multicenter national study. J Thorac Cardiovasc Surg, 130:1616-22.
[27] Santambrogio L, Nosotti M, Baisi A, Ronzoni G, Bellaviti N, Rosso L (2001). Pulmonary lobectomy for lung cancer: a prospective study to compare patients with forced expiratory volume in 1 s more or less than 80% of predicted. Eur J Cardiothorac Surg, 20:684-7.
[28] Varela G, Brunelli A, Rocco G, Marasco R, Jiménez MF, Sciarra V, Aranda JL, Gatani T (2006). Predicted versus observed FEV1 in the immediate postoperative period after pulmonary lobectomy. Eur J Cardiothorac Surg, 2006; 30:644-8.
[29] Favier R, Kepenkian G, Desplanches D, Flandrois R (1982). Effects of chronic lung denervation on breathing pattern and respiratory gas exchange during hypoxia, hypercapnia and exercise. Respir Physiol, 47:107-19.
[30] Robles AM, Shure D (2004). Optimization of lung function before pulmonary resection: pulmonologists’ perspectives. Thorac Surg Clin, 14:295-304.
[31] Tantucci C, Duguet A, Similowki T, Zelter M, Derenne J-Ph, Milic-Emili J (1998). Effect of salbutamol on dynamic hyperinflation in chronic obstructive pulmonary disease patients. Eur Rspir J, 12:799-804.
[32] O’Donnell DE (1994). Breathlessness in patients with chronic airflow limitation. Mechanisms and management. Chest, 106:904-12.
[33] Diaz O, Villafranca C, Ghezzo H, Borzone G, Leiva A, Milic-Emil J, Lisboa C (2000). Role of inspiratory capacity on exercise tolerance in COPD patients with and without expiratory flow limitation at rest. Eur Respir J, 16:269-75.
[34] Matsuo M, Hashimoto N, Usami N, Imaizumi K, Wakai K, Kawabe T, Yokoi K, Hasegawa Y (2012). Inspiratory capacity as a preoperative assessment of patients undergoing thoracic surgery. Interact Cardiovasc Thorac Surg, 14:560-4.
[35] Rajendran AJ, Pandurangi UM, Murali R, Gomathi S, Vijayan VK, Cherian KM (1998). Pre-operative pulmonary rehabilitation for patients of chronic obstructive pulmonary disease undergoing coronary bypass graft surgery. Indian Heart J, 50:531-4.
[36] Cerfolio RJ, Bryant AS, Singh S, Bass CS, Bartolucci AA (2005). The management of chest tubes in patients with a pneumothorax and an air leak after pulmonary resection. Chest, 128:816-20.
[37] Varela G, Brunelli A, Jiménez MF, Di Nunzio L, Novoa N, Aranda JL, Sabbatini A (2010). Chest drainage suction decreases differential pleural pressure after upper lobectomy and has no effect after lower lobectomy. Eur J Cardiothorac Surg, 37:531-4.
[38] Sekine Y, Iwata T, Chiyo M, Yasufuku K, Motohashi S, Yoshida S, Suzuki M, Iizasa T, Saitoh Y, Fujisawa T (2003). Minimal alteration of pulmonary function after lobectomy in lung cancer patients with chronic obstructive pulmonary disease. Ann Thorac Surg, 76:356-62.
[39] Beccaria M, Corsico A, Fulgoni P, Zoia MC, Casali L, Orlandoni G, Cerveri I (2001). Lung cancer resection: the prediction of postsurgical outcomes should include long-term functional results. Chest, 120:37-42.
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