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REVIEW PAPER

Impact of Video-Assisted Thoracoscopic Major Lung Resection on Immune Function

Calvin SH Ng, MD, Innes YP Wan, FRCS, Anthony PC Yim, DM

Division of Cardiothoracic Surgery, The Chinese University of Hong Kong, Prince of Wales Hospital Hong Kong, China

Anthony PC Yim, DM Tel: +852 2632 2629 Fax: +852 2637 7974 Email: yimap{at}cuhk.edu.hk, Department of Surgery, The Chinese University of Hong Kong, Prince of Wales Hospital, Hong Kong, China.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 INFLAMMATORY AND...
 SYSTEMIC CELLULAR IMMUNITY
 POSTOPERATIVE IMMUNE STATUS:...
 FUTURE PERSPECTIVES
 REFERENCES
 
Video-assisted thoracoscopic major lung resection for early stage non-small-cell lung carcinoma has been associated with less postoperative pain, better preserved pulmonary function, shorter hospital stay, and enhanced tolerance of adjuvant chemotherapy compared to thoracotomy. Initial concerns regarding safety, oncological clearance, and cost effectiveness were unfounded. Several recent trials have reported improved long-term survival in patients with early stage non-small-cell lung carcinoma undergoing video-assisted thoracoscopic major lung resection, compared to the open technique, although there are inconsistencies. Interestingly, the immune status and autologous tumor killing ability of lung cancer patients have previously been associated with long-term survival. Video-assisted thoracoscopic lung resection results in an attenuated postoperative inflammatory response, but more importantly, it better preserves postoperative immune function. Circulating natural killer and T-cell numbers, T-cell oxidative activity, and levels of immunochemokines such as insulin growth factor binding protein-3 are higher after video-assisted thoracoscopic surgery than after thoracotomy. Recently, interest has developed in the role of the angiogenesis factor, vascular endothelial growth factor, after cancer surgery. Whether differences in immunological and biochemical mediators contribute towards improved long-term survival following video-assisted thoracoscopic major lung resection for cancer remains to be confirmed.

Key Words: Immune System • Lung Neoplasms • Thoracic Surgery • Video-Assisted


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
INFLAMMATORY AND...
 SYSTEMIC CELLULAR IMMUNITY
 POSTOPERATIVE IMMUNE STATUS:...
 FUTURE PERSPECTIVES
 REFERENCES
 
In the past decade, video-assisted thoracic surgery (VATS) has undergone significant evolution and refinement, and continues to change the way thoracic conditions are managed. VATS major lung resection (lobectomy or pneumonectomy) for early stage lung cancer has now gained acceptance, but some surgeons remain skeptical about its safety, oncological clearance, long-term benefits, and cost effectiveness. Over the past few years, these concerns have largely been shown to be unfounded.1,2 It is well accepted than VATS major lung resection can be associated with less postoperative pain, better preserved pulmonary and shoulder function, as well as shorter hospital stay compared to the thoracotomy approach.2,3 More recently, studies have suggest that following VATS lobectomy for cancer, patients were better equipped to tolerate adjuvant chemotherapy, resulting in a higher compliance rate, fewer delays, and reduced doses of chemotherapy.3,4 Interestingly, several nonrandomized studies have also shown a trend towards improved intermediate to long-term survival in favor of VATS for early non-small-cell lung carcinoma (NSCLC) compared to the open technique.1,2,5,6 However, it should be noted that this apparent survival advantage has not been consistently demonstrated.7,8 Furthermore, there is growing evidence to suggest that the body’s immune function is better preserved after VATS compared to thoracotomy, as documented by the release of pro-and antiinflammatory cytokines, immunomodulatory cytokines, circulating T cells (CD4) and natural killer (NK) cells, and lymphocyte function.9 As immunosurveillance is believed to be important in tumor suppression, surgically induced immunosuppression may predispose to increased tumor growth and recurrence (Figure 1Go).9 Most cases of lung cancer recurrence are at a distance from the primary tumor site, and most cancers that recur are likely to be metastatic at initial exploration. Hence, the use of VATS for lung cancer resection may allow better preservation of host immunity and optimize long-term survival. The latest studies in this area are reviewed.


Figure 1
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  		Figure 1. Immune parameters influenced by major lung resection surgery.

 

   INFLAMMATORY AND IMMUNOMODULATORY CYTOKINES
TOP
 ABSTRACT
 INTRODUCTION
 INFLAMMATORY AND...
SYSTEMIC CELLULAR IMMUNITY
 POSTOPERATIVE IMMUNE STATUS:...
 FUTURE PERSPECTIVES
 REFERENCES
 
Surgical trauma has long been known to cause a systemic inflammatory cytokine response, resulting in increased circulating levels of interleukin (IL)-1, IL-6, and tumor necrosis factor-{alpha}.10 Furthermore, studies comparing open and minimal access techniques for abdominal surgery have demonstrated an attenuated inflammatory response in serum IL-6 and C-reactive protein with the latter approach.9,11,12 Similarly, the reduced access trauma of VATS major lung resection compared with open thoracotomy resulted in reduced postoperative C-reactive protein, IL-6, and IL-8 responses13–15 However, no differences in postoperative tumor necrosis factor-{alpha} or IL-1β levels were observed between the 2 approaches.14 Recently, it has been shown that the postoperative difference in levels of IL-6 between the 2 approaches is more likely related to difference in access trauma rather than the extensiveness of the intrathoracic procedure.16 Interestingly, VATS lobectomy was also associated with reduced release of the antiinflammatory cytokine IL-10 in the early postoperative period, compared to thoracotomy.14 This finding may be important because IL-10, in addition to being a T-helper type 2 (Th-2) cytokine which generally suppress cell-mediated immunity, can help tumor cells evade the host immune system by direct inhibition of NK cell-mediated cytotoxicity and increase the resistance of certain tumor cell lines to NK cell destruction.17

Apart from being a marker of surgical trauma, IL-6 may also play a role in postoperative immunosuppression via its effects on IL-1β and tumor necrosis factor-{alpha} production, which are necessary for effective cellular immunity and immunosurveillance.18 In addition, elevated plasma levels of IL-6 can encourage proliferation of certain subtypes of NSCLC, promote insulin growth factor (IGF) activation, and cause insulin growth factor binding protein (IGFBP)-3 inhibition, thereby contributing to an environment favoring tumor growth.9,19 Immunomodulatory cytokine IGF-1 is known to facilitate progression of numerous tumors due to its ability to stimulate cancer proliferation and reduce cancer cell apoptosis.20 IGFBP-3 on the contrary, by being a natural antagonist of IGF-1, binds and attenuates the activity of IGF-1, thereby exerting antitumorigenesis properties. Furthermore, IGFBP-3 can independently induce apoptosis in many colonic, prostatic, and certain NSCLC cell lines, as well as impair DNA synthesis in some poorly differentiated tumor cells.9,21,22 These properties of IGFBP-3 may be important after lung cancer resection when tumor cells may be shed into the circulation.7 In a recent prospective study of patients with early stage NSCLC undergoing major lung resection, VATS was associated with higher levels of IGFBP-3 in the early postoperative period compared to thoracotomy (Figure 2AGo).23 However, no clinical benefit was found in VATS patients during the short postoperative follow-up period. Furthermore, the blood levels of another immunochemokine, matrix metalloproteinase (MMP)-9, which is released from mononuclear cells in association with surgical trauma, were reciprocally lower in patients who underwent VATS major lung resection (Figure 2BGo).23,24 Apart from the ability of MMP-9 to cleave and deactivate IGFBP-3, MMP-9 may also facilitate tumor invasion and metastasis via its proteolytic activity against type IV collagen of the basement membrane.23–26 Early postoperative differences in the levels of these inflammatory cytokines and immunochemokines between the surgical approaches may have important implications for tumor cell behavior.


Figure 2
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  		Figure 2. Plasma levels of (A) IGFBP-3 and (B) MMP-9 in patients undergoing video-assisted thoracoscopic and open major lung resection for early stage non-small-cell lung cancer. Data are given as median ± interquartile range, with intergroup differences. BS = before surgery, POD = postoperative day.

 

   SYSTEMIC CELLULAR IMMUNITY
TOP
 ABSTRACT
 INTRODUCTION
 INFLAMMATORY AND...
 SYSTEMIC CELLULAR IMMUNITY
POSTOPERATIVE IMMUNE STATUS:...
 FUTURE PERSPECTIVES
 REFERENCES
 
Major surgery can affect multiple immune parameters, including those components involved in cellular immunity, which may have an impact on postoperative infection and tumor immunosurveillance. Most studies so far on postoperative cell-mediated immunosuppression have been based on open and laparoscopic abdominal surgery.9 Disturbances in cellular immunity that are found postoperatively include decreased lymphocyte proliferation, changes in the circulating blood lymphocyte subsets, downregulation of Th-1 cytokine response, which favors humoral rather than cellular immunity, and decreased delayed type hypersensitivity responses.27–29 In comparison, only limited studies have been conducted so far on the effects of major lung resection surgery on postoperative cellular immunity (Table 1Go).


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  		Table 1. Clinical studies comparing systemic cellular immune responses after VATS and open thoracotomy lobectomy for bronchogenic carcinoma
 
VATS lobectomy in patients with early stage NSCLC was shown to result in less immunosuppression of lymphocyte activity and less suppression of numbers of lymphocytes, total T cells, and CD4 T cells in the early postoperative period compared to open thoracotomy.18,30 Furthermore, by postoperative day 7, NK cell numbers were found to be significantly higher following VATS lobectomy compared to the open approach, suggesting that VATS is associated with a quicker NK cell recovery than conventional thoracotomy.18,30 NK cells are known to play a significant role in tumor immunosurveillance through their ability to recognize, target, and directly destroy tumor cells without prior sensitization. In the context of lung tumor surgery, less suppressed cellular immunity during the early postoperative period may confer a lower predisposition to tumor growth and recurrence. It is of interest to note that the neutrophil phagocytic activity in terms of reactive oxygen species production was less affected after VATS major lung resection than after thoracotomy.13 The relationship between cellular immunity, cytokines and plasma immunomodulatory mediators is undoubtedly very complex and will need further evaluation. It should be highlighted that the differences in almost all of the postoperative immune parameters measured thus far between VATS and thoracotomy groups are short lived, in the order of hours to a few days. Thus one should be excited but cautious in relating these findings to survival benefits following VATS lobectomy for NSCLC. Furthermore, the clinical importance of better preserved immune function following VATS has yet to be proved in the setting of a generally healthy patient population that is immunocompetent preoperatively.


   POSTOPERATIVE IMMUNE STATUS: DOES IT MAKE A DIFFERENCE?
TOP
 ABSTRACT
 INTRODUCTION
 INFLAMMATORY AND...
 SYSTEMIC CELLULAR IMMUNITY
 POSTOPERATIVE IMMUNE STATUS:...
FUTURE PERSPECTIVES
 REFERENCES
 
Currently, there is no study that links a better-preserved immune status following VATS lung resection for early stage NSCLC to any significant survival benefit. The difficulty in demonstrating such a relationship is that a large randomized trial measuring multiple postoperative immune function markers and long-term survival after VATS and open lobectomy is needed. Such a trial is unlikely to happen because of the logistics associated with large-scale immune function measurements, as well as the difficulty of well-established VATS centers to randomize patients into a thoracotomy group, when patient choice often precludes the open approach.

In the past, numerous immunological parameters have been investigated as potential prognostic factors in lung cancer. For example, delayed hypersensitivity skin testing and lymphoblastogenesis induced by mitogens have been correlated with survival in lung cancer patients.31,32 Interestingly, in primary resected NSCLC patients, the postoperative lymphocyte autologous tumor-killing (ATK) and NK cell activity during the 2 weeks immediately after surgery was an important prognostic factor.33,34 Leukocytes identified to be involved in ATK include CD3(+), CD4(–), CD8(+), and CD11 b(–).34 Those patients with higher postoperative ATK had significantly lower 5-year tumor recurrence rates as well as better survival.34 Furthermore, such association between survival and ATK was present in both early and advanced stage NSCLC.34 More recently, Nakamura and colleagues35 prospectively measured various cellular immunologic parameters including lymphocyte subsets, NK cell activity and lymphoblastogenesis stimulation in peripheral blood samples taken from patients before the initiation of therapy (surgery or chemotherapy). The study found no significant survival differences associated with lymphoblastogenesis, NK activity, CD16+ T cells, CD3, CD4, CD8 and CD4/CD8 ratio. However, upon subgroup analysis according to histologic type, an increase of human leukocyte antigen-D-related+ cells and the CD16+ T-cell subset suggested a worse prognosis in squamous cell carcinoma. Similarly, an increase in human leukocyte antigen-D-related+ cells and also a decreased CD4/CD8 ratio were associated with a worse prognosis in small-cell carcinoma.35,36 Lately, it has been found that a high interferon-gamma+/CD4+ to IL-4+/CD4+ lymphocyte cell ratio in peripheral blood was also associated with a poor 5-year prognosis in NSCLC patients.37 There is certainly some evidence to suggest that certain immunity parameters are associated with survival in lung cancer patients, the importance of which may vary according to histologic type. Whether this association may partly explain the rare phenomenon of spontaneous tumor regression in squamous cell and small cell carcinoma and improved survival in early stage NSCLC patients following VATS major lung resection warrants further investigation.38,39


   FUTURE PERSPECTIVES
TOP
 ABSTRACT
 INTRODUCTION
 INFLAMMATORY AND...
 SYSTEMIC CELLULAR IMMUNITY
 POSTOPERATIVE IMMUNE STATUS:...
 FUTURE PERSPECTIVES
REFERENCES
 
Major lung resection has so far been shown to produce significant alterations in certain inflammatory and immunomodulatory cytokines and cellular immune responses. In addition to IL-6, IL-10, IGFBP-3, and MMP-9, which may be partly responsible for postoperative immunosuppression, other mediators of interest include IL-12, IL-17, IL-23, and IL-25 (IL-17E). Interleukins 12, 17, and 23 are important in T-cell-dependent immune responses, mobilization of NK cells and neutrophils.40 More specifically, IL-12 can also increase interferon-{gamma} production and induce the development of Th1-type cells from naive helper T-lymphocytes.41 Because the ratio of Th1 to Th2 cells can impact upon survival in NSCLC patients, IL-12 may be an important immunomodulatory cytokine. IL-25 (IL-17E) is a novel inflammatory cytokine that was recently shown to possess significant immunomodulatory properties through activation of eosinophils.37 Following activation, eosinophils produce a variety of cytokines, such as eotaxin, which demonstrate antitumor activities.42 Undoubtedly, there are many other undiscovered surgery-influenced chemokines or factors that impact on tumor growth and development after surgery. However, it is notable that little attention has been paid to angiogenesis in the postoperative period. Vascular endothelial growth factor (VEGF) is the most potent inducer of angiogenesis found to date; it is necessary for wound healing but also acts as a strong tumor growth promoter. The release of VEGF after surgery could have undesirable effects on residual tumor cells, and may enhance tumor growth and metastasis formation. Belizon and colleagues43,44 found elevated plasma levels of VEGF from several days after major abdominal surgery up to at least 4 weeks postoperatively. Furthermore, the postoperative VEGF levels were significantly higher in patients who underwent laparotomy compared to the laparoscopic approach to colectomy, irrespective of whether surgery was for benign or malignant pathology.44 Similar differences may also be found in patients undergoing VATS and open major lung resection. It should be pointed out that in addition to ex-vivo measurements, the clinical impact of these cytokines and factors will require in-vitro assays to determine whether postoperative plasma stimulates tumor proliferation and invasion.

Apart from access trauma per se, other factors favoring VATS lung resection, such as reduced postoperative pain, may better preserve cellular immunity by reducing lymphocyte suppression and attenuating the proinflammatory cytokine response.45 Furthermore, because VATS major lung resection is not a uniform approach, differences in VATS technique, for example the use of and size of a utility thoracotomy, rib spreading, and segmental rib resection, as well as the duration of surgery, may have addition effects on the postoperative inflammatory response.8,46 These exciting areas also await future investigations.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 INFLAMMATORY AND...
 SYSTEMIC CELLULAR IMMUNITY
 POSTOPERATIVE IMMUNE STATUS:...
 FUTURE PERSPECTIVES
 REFERENCES
 

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Asian Cardiovasc Thorac Ann 2009; 17:426-432
© 2009 by SAGE Publications
DOI: 10.1177/0218492309338100



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