Gen Thorac Cardiovasc Surg (2014) 62:24–30 DOI 10.1007/s11748-013-0346-x

CURRENT TOPICS REVIEW ARTICLE

Long-term pulmonary function after major lung resection Kazuhiro Ueda • Masataro Hayashi • Nobuyuki Tanaka • Toshiki Tanaka • Kimikazu Hamano

Received: 4 October 2013 / Published online: 23 November 2013 Ó The Japanese Association for Thoracic Surgery 2013

Abstract The function of the remaining lungs after major lung resection may be a determinant of the early postoperative outcome, as well as the late postoperative quality of life of the patient. Thus, extensive efforts have been made to accurately estimate the postoperative pulmonary function using a variety of methods: the segment counting method is utilized in patients without parenchymal diseases, while the functional lung imaging technique may be useful in patients with heterogeneous anatomical lung diseases. The postoperative pulmonary function is influenced not only by the extent of parenchymal resection, but also by various other factors, such as the site of resection, the mode of thoracotomy, the severity of pulmonary emphysema and/or the postoperative progression of pulmonary fibrosis. Although thoracoscopic surgery or segmental resection can lessen the extent of chest wall damage or the extent of parenchymal resection compared with conventional operations, the resulting functional benefits do not last. Interestingly, the postoperative pulmonary function continues to improve during the first postoperative

This review was submitted at the invitation of the editorial committee. K. Ueda (&)  M. Hayashi  K. Hamano Department of Surgery and Clinical Science, Division of Chest Surgery, Yamaguchi University Graduate School of Medicine, 11-1 Minami-Kogushi, Ube, Yamaguchi 755-8505, Japan e-mail: [email protected] N. Tanaka Department of Radiopathology and Science, Division of Radiology, Yamaguchi University Graduate School of Medicine, 1-1-1 Minami-Kogushi, Ube, Yamaguchi 755-8505, Japan T. Tanaka Department of Thoracic Surgery, NHO Yamaguchi-Ube Medical Center, 685 Higashi-kiwa, Ube 755-0241, Japan

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year as if the remaining lungs grow, although the cause(s) of this compensatory response of the remaining lungs remains unclear. Such an ability of the remaining lung to compensate for the lost lung function may eventually determine the late postoperative pulmonary function. Keywords Pulmonary function  Lobectomy  Segmentectomy  Compensatory lung growth

Introduction The function of the remaining lungs after major lung resection may be a determinant of the early postoperative outcome, as well as the late postoperative quality of life of the patients [1–3]. Therefore, an assessment of the pulmonary ventilatory capacity is mandatory in patients undergoing major lung resection [1]. Because the adult lung generally does not have the ability to regenerate new alveolar septal tissues [4], the postoperative pulmonary function can be theoretically determined by the amount of parenchymal resection. However, the postoperative pulmonary function can be also influenced by various other factors, such as the site of resection (upper lobectomy or lower lobectomy), the severity of pulmonary emphysema, the surgical approach (open or port-access), and whether the patient receives bronchoplasty or induction chemoradiotherapy. Furthermore, the postoperative pulmonary function is time-dependently altered during the first year after the operation. Therefore, there is a considerable discrepancy between the preoperatively predicted pulmonary function that will remain postoperatively and the actual late postoperative pulmonary function. Knowledge of these issues may be beneficial for the therapeutic decisionmaking for patients with resectable lung cancer.

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Time-trends in postoperative pulmonary function The postoperative pulmonary function is impaired extensively just after major resection, and recovers timedependently. The impairment is mainly due to the effects of general anesthesia and the chest wall damage. General anesthesia itself results in a relaxation of the respiratory muscles, leading to a reduction in the functional residual lung volume [5]. This reduction likely results in the collapse of the small airways, thus causing microatelectasis, especially in patients with chronic obstructive pulmonary disease (COPD) [5, 6]. These alterations are the main pathology of postoperative hypoxemia, and persist for several days postoperatively. The postoperative pulmonary function is also impaired due to the reduction in the chest wall compliance induced by thoracotomy. Therefore, the early postoperative ventilatory capacity is lower than the predicted values [7]. With the improvement of the chest wall mobility due to wound healing, the postoperative ventilatory capacity improves time-dependently: the postoperative ventilatory capacity is generally better than the predicted values 3 months after lobectomy [8, 9], and continues to improve significantly during the subsequent several months [9]. The postoperative ventilatory capacity becomes maximal between 6 and 12 months after lobectomy, without further improvement [10, 11]. Interestingly, after heart–lung transplantation, the recovery of the pulmonary ventilatory capacity is also maximal between 6 and 9 months postoperatively [12]. However, clinicians must aware of the probable effect of a selection bias on the assessment of the late postoperative (i.e., 6 or 12 months) pulmonary function: patients who did not present at followup examination should presumably be considered to be the patients with worse conditions, and prolonging the last evaluation time could falsely improve the results [7, 8]. In contrast to the time-trend results after lobectomy, Bolliger et al. [9] found no significant improvement of the ventilatory capacity between 3 and 6 months after pneumonectomy. Such findings may have arisen because the chest wall trauma is not significantly associated with the deterioration of the remaining lung function after pneumonectomy. Interestingly, the ventilatory capacity improves relatively slowly until some years after pneumonectomy in some patients, probably due to lung growth [13, 14].

Extent of the loss in the pulmonary function after lobectomy It has been considered that the extent of the loss of pulmonary function after lobectomy is proportional to the amount of parenchymal resection [3]. However, as

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mentioned above, the function of the remaining lung after lobectomy improves time-dependently during the first postoperative year. Zeiher et al. [15] reported that the late postoperative forced expiratory volume in 1 s (FEV1) was 250 ml higher than the values predicted by the standard segment counting technique. Table 1 shows the percent change in the preoperative to late postoperative pulmonary function. The FEV1 was reduced by 8.8–17.6 % of the preoperative values after lobectomy [8, 9, 11, 16–18], although lobectomy corresponded to resection of, on average, 20 % of the total lung parenchyma. Regardless of the significant reduction in the FEV1, the diffusing capacity of the lung for carbon monoxide (DLCO) and the maximum oxygen consumption (VO2max) did not decrease or only slightly decreased after lobectomy [8, 9, 16, 17]. Likewise, Pelletier et al. [19] reported that the exercise capacity, as measured by an ergometer, did not deteriorate after lobectomy. Regardless of some conflicting reports [16, 20], the assessment of postoperative pulmonary function by means of the FEV1 can likely lead to an overestimation of the loss of the postoperative pulmonary function.

Modalities for predicting the postoperative pulmonary function The segment counting method, which consists of counting the number of functioning segments that will be resected and the number of total functioning segments, is the most feasible way to predict the postoperative pulmonary function [3]. However, this method is based on the hypothesis that every functioning segment in each patient contributes equally to the respiration. In patients with heterogeneous anatomical lung disease, perfusion scintigraphy has been utilized to evaluate the functional contribution of the affected lung that will be resected. With the technological development, perfusion scintigraphy enabled the accurate detection of small perfusion defects by projecting the images during breath-holding, and facilitates accurate outlining of the lung area that will be resected by using integrated images with the same respiratory phase computed tomography (CT). This revised technique contributes to more accurate prediction of the postoperative pulmonary function, compared with conventional scintigraphy [21, 22]. There are some other radiologically based methods that can be used to predict regional lung function, including the use of quantitative CT [23, 24], perfusion magnetic resonance imaging (MRI) [25] or dual energy CT [26]. However, these modalities should be used in selected patients who have limited functional reserve, because good agreement was observed between the values predicted by segment

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Table 1 The percent difference in the long-term pulmonary function after lobectomy compared to the preoperative values Authors

Bolliger

Wang

Nagamatsu

Brunelli

Ginsberg

Funakoshi

Postoperative evaluation (months)

6

12

12

3

6

12

Number of patients

50

19

18

180

67

80a

FVC

-7.3

-14.0

-17.3

N/A

-5.9

-18.9

FEV1

-8.8

-10.6

-17.6

-16

-9.1

-17.6

DLCO

-4.0b

-3.6

-5.0

-11.5

N/A

N/A

VO2peak

-1.0b

-11.8

0b

-3.0

N/A

N/A

Values are expressed as the numbers or % change from the preoperative evaluation to the postoperative evaluation Including 11 patients who received preoperative induction therapy

a

b

No significant difference vs. the preoperative data

counting and those predicted by radiological techniques in patients with normal lungs [27, 28].

Determinants of the postoperative pulmonary function Amount of lung resected In general, the postoperative pulmonary function is determined by the amount of lung parenchyma that is resected. However, because the pulmonary function alters to various degrees in the early postoperative period, the late postoperative pulmonary function is not closely related to the amount of resection in patients undergoing lobectomy. Indeed, Brunelli et al. [29] reported that the postoperative VO2max, as measured 3 months after lobectomy, could not be predicted by the amount of resection. Therefore, it may be important to identify the other determinants of the postoperative pulmonary function, besides the amount of resection. Resection mode (pneumonectomy/lobectomy/ segmentectomy) Most reports suggest that lobectomy contributes to preserving the pulmonary function, as measured by the forced vital capacity (FVC), FEV1, DLCO, VO2max, and exercise capacity, compared with pneumonectomy [8, 9]. Likewise, many reports suggest that segmentectomy contributes to preserving the ventilatory capacity, as measured by the FEV1, compared with lobectomy [18, 30–33]. However, there is little evidence indicating that segmentectomy contributes to preserving the DLCO, VO2max and exercise capacity, compared with lobectomy [30], probably because these variables are not remarkably deteriorated even after lobectomy, as mentioned above. We previously evaluated the CT-based functional lung volume, which represents the lung volume of normal attenuation (-600 to -910 HU) in patients undergoing segmentectomy or lobectomy [34].

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Unfortunately, we found no significant advantage of segmentectomy for preserving the functional lung volume compared with lobectomy. Although segmentectomy could spare several segments in the affected lobe, the spared segments shrunk to some degree during the late postoperative period compared with the baseline [34, 35]. Considering that the assessment of the postoperative pulmonary functional loss by means of the FEV1 can exaggerate the postoperative functional loss, as mentioned before, segmentectomy may have only subclinical effects on the preservation of the remaining lung function during the late postoperative period, although selected patients who have a risk of receiving lobectomy due to compromised pulmonary function may benefit from the segmentectomy. Bronchoplasty Stenosis of the anastomosis site after bronchial sleeve resection can lead to a deterioration of the pulmonary ventilatory capacity. However, according to the literature, the pulmonary function after sleeve lobectomy is comparable to that after standard lobotomy [36, 37]. Therefore, if the sleeve lobectomy can be oncologically acceptable, avoiding pneumonectomy may contribute to preserving the pulmonary function. Induction chemo-radiotherapy It has been recognized that induction chemo-radiotherapy induces a reduction in the preoperative pulmonary function [38], probably because of the toxic effects of the treatment on the affected lobe or lung. Interestingly, Granone et al. [39] reported that the extent of the loss in the pulmonary function after lobectomy was enhanced in patients receiving induction therapy, as compared with patients not receiving induction therapy, which was in accordance with the report by Funakoshi et al. [11]. Although the exact mechanisms remain unknown, induction therapy might

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play a part in disturbing the recovery or improvement of the function of the remaining lung after lobectomy.

ventilatory capacity, was observed in a proportion of patients who had undergone upper lobectomy [44].

Site of resection (upper/lower lobectomy)

The presence of COPD

Which type of lobectomy is most advantageous for the remaining lung in terms of the recovery or improvement of the ventilatory function (upper or lower lobectomy) has been unclear [40, 41], because the mechanisms underlying the improvement in the remaining lung function are multifactorial. For instance, patients with upper lobe-predominant emphysema are likely to undergo a volume reduction effect after upper lobectomy. Upper lobectomy may adversely affect the remaining lung function, because the remaining middle or lower lobe may be influenced by the anatomical rearrangement, which can act on the narrowing or kinking of the lobe or main-stem bronchus (Fig. 1). We previously performed an anatomical-functional analysis using quantitative CT and spirometry in patients without significant emphysema undergoing upper lobectomy or lower lobectomy [42]. As a result, although lower lobectomy implied greater parenchymal resection than upper lobectomy, the postoperative ventilatory function and functional lung volume, which are indicated by normal CT attenuation, were comparable. These results are consistent with some other reports [8, 43]. Significant bronchial kinking, which leads to the deterioration of the

It has been well recognized that the postoperative pulmonary function can be unexpectedly improved after lobectomy due to a volume reduction effect in patients with moderate to severe pulmonary emphysema. Relief of the airflow obstruction, improved respiratory muscle function, elimination of dead space ventilation in ventilated but unperfused areas, and improved cardiovascular hemodynamics may all contribute to this unexpected improvement [45–47]. Many reports emphasize that the remaining lung function is higher than the predicted values in patients with COPD [40, 41, 48]. However, the extent of the differences between the predicted and measured postoperative pulmonary function differs greatly in individual patients with COPD. We found that the patients with a certain degree of low-attenuation areas in the lung field, as measured by quantitative CT, rather than the patients with airflow limitation alone, are likely to be affected by the volume reduction effect [23]. The grading of emphysema by quantitative CT may be helpful in decision-making for the surgical treatment of patients with resectable lung cancer who have compromised pulmonary function. Surgical approach (VATS/open thoracotomy)

Preoperative

Post-right upper lobectomy

B1 B6 B2 B4+5

B3

B8 B4+5

B6

B9 B8

B9

B10

B10

Fig. 1 The three-dimensional computed tomography volume rendering image of the central airways, with special reference to the right hemithorax. Compared with the preoperative image, right upper lobectomy induced the sigmoidal curvature of the right main-stem bronchus to the bronchus intermedius. Note that the middle lobe bronchus is kinked. These alterations are due to the upward movement of the remaining middle and lower lobes after upper lobectomy

The ventilatory capacity is impaired during the early postoperative period in accordance with the level of chest wall trauma (posterolateral thoracotomy [ anterior thoracotomy [ video-assisted thoracic surgery) due to the reduction in the chest wall motility [49]. Many reports suggest that the pulmonary ventilation capacity is better preserved after lobectomy via video-assisted thoracic surgery than after posterolateral thoracotomy within 3 months after the operation [50–52]. However, the differences may decrease or disappear 1 year after lobectomy [52].

Improvement of the pulmonary function after major resection Major lung resection induces the expansion of the remaining lung, so that the remaining lungs match the thoracic cavity. In rodents, the postoperative enlargement of the remaining lung is accompanied by alveolar multiplication, which is known as compensatory lung growth. Hsia et al. [53] reported that compensatory lung growth is observed even in adult dogs after right pneumonectomy. In contrast to the experimental animals, it remains controversial whether compensatory lung growth occurs in

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human adults, because it may be difficult to evaluate the changes in the amount of the alveolar septal tissues between the preoperative and the postoperative lungs. According to a literature, a remarkable case of extensive enlargement of the remaining lung occurred in a 35-yearold female who had all but the right upper lobe resected because of bronchiectasis [13]. Although the volume of the remaining right upper lobe did not reach normal, it seems likely that considerable lung growth, and probably even alveolar multiplication, occurred. Recently, Butler et al. [14] showed evidence of compensatory lung growth in a 33-year-old female by means of MRI with the use of hyperpolarized helium-3 gas. Regardless of these exceptional cases, the majority of the elderly patients undergoing major lung resection for cancer have little or only limited potential for compensatory lung growth. The postoperative enlargement of the remaining lung has been attributed to simple hyperinflation of the individual alveolar units. Particularly after a pneumonectomy in adult patients, the extensive enlargement of the contralateral lung occasionally causes exertional dyspnea, instead of improving the ventilatory capacity, due to the resultant mediastinal shift, which can contribute to narrowing the central airways or pulmonary vessels by kinking or compression by the existing mediastinal structures or vertebral bodies [54, 55]. This adverse event is known as post-pneumonectomy syndrome, and is predominantly observed in patients who are younger or female [54]. Macare0 van Maurik et al. [54] suggested that younger and female patients have relatively elastic mediastinal tissues, which likely cause excessive mediastinal shifting. However, considering that these patients can have lungs with the potential for growth, post-pneumonectomy syndrome, especially that occurring in younger female patients, can be a result of compensatory lung growth. Of note, post-pneumonectomy syndrome is not induced in patients with elastic mediastinum, but in patients whose lungs have the ability to enlarge extensively, probably due to growth. Interestingly, Hsia et al. [56] reported that prevention of the mediastinal shift after pneumonectomy in dogs caused impairment of the compensatory growth of the remaining lung. Further attempts should be made to clarify the pathophysiology of adult lung growth and post-pneumonectomy syndrome in humans. Interestingly, although compensatory lung growth includes the reproduction of new alveolar septal tissues, the postoperative ventilatory capacity will not improve correspondingly because the airways show less compensatory growth than the lung parenchyma, which leads to so-called dysanaptic lung growth [57]. We, therefore, believe that compensatory lung growth in adult patients cannot be diagnosed by means of the pulmonary ventilatory capacity, but that it may be possible using radiopathological evaluation techniques.

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We previously evaluated the lung volume of normal attenuation (-600 to -910 HU) on CT as a surrogate for the normal lung parenchyma, in combination with the ventilatory capacities determined by spirometry in patients undergoing major lung resection for cancer. As a result, the postoperative lung volume was 13 % higher than the predicted postoperative values, while the postoperative FVC and FEV1 were only 6 and 10 % higher than the predicted postoperative values, respectively [34]. Although all these postoperatively measured values were better than the predicted values, the percent changes in the ventilatory capacities (FVC and FEV1) were not closely dependent on the percent change in the lung volume (R = 0.51 for the lung volume change and the FVC change, R = 0.61 for the lung volume change and the FEV1 change) [34]. These results may suggest that the ventilatory capacity is not necessarily a reliable marker of a compensatory lung response. Similar to our study, Mizobuchi et al. [58, 59] estimated lung weight, in combination with lung volume, radiologically by chest CT. They also found that the CTbased lung volume and weight of the remaining lung after major lung resection were significantly higher than the predicted values, suggesting occurrence of compensatory phenomena of the remaining lung. Although the increased lung volume and weight do not always mean that there has been lung growth, a comprehensive assessment with a radiopathological technique should be performed to clarify the role of the compensatory lung growth in postoperative patients, because it may eventually lead to improvement of the preoperative risk assessment of patients with resectable lung diseases.

Conclusions The function of the remaining lung after major resection is impaired immediately after the operation, but improves subsequently during the first postoperative year, and usually becomes higher than the predicted postoperative values. The improvement of the postoperative pulmonary function may be, at least partly, linked to the enlargement of the remaining lung (the compensatory lung response). The eventual postoperative pulmonary function is influenced not only by the extent of lung resection, but also by various other factors. Interestingly, the eventual postoperative pulmonary function, especially the gas exchange capacity and the exercise capacity, is by far better than the predicted values after lobectomy. Therefore, measurement of the postoperative FEV1 alone can underestimate the real pulmonary function after a lobectomy. Such a discrepancy between the ventilatory capacity and the gas exchange capacity or exercise capacity may be due to the disproportionate response between the conductive airways and the alveolar tissues. The

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potential of the remaining lung with regard to the compensatory response may eventually determine the postoperative pulmonary function, as well as the quality of life of the patients. A comprehensive analysis of the structural changes in the remaining lung using radiopathological techniques will thus be indispensable to clarify these issues. Conflict of interest interest exists.

The authors have declared that no conflict of

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Long-term pulmonary function after major lung resection.

The function of the remaining lungs after major lung resection may be a determinant of the early postoperative outcome, as well as the late postoperat...
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