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Division of Cardiothoracic Surgery, University of Alabama at Birmingham, Birmingham, Alabama
Accepted for publication April 23, 2008.
* Address correspondence to Dr Cerfolio, Department of Surgery, Division of Cardiothoracic Surgery, University of Alabama at Birmingham, 703 19th St S, ZRB 739, Birmingham, AL 35294 (Email: rcerfolio{at}uab.edu).
Presented at the Forty-fourth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2008.
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Abstract |
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Methods: This retrospective cohort study used a prospective database. Patients who had biopsy-proven, nonbulky N2 disease underwent neoadjuvant chemoradiotherapy and were restaged or resected, or both.
Results: There were 402 patients, and 326 (81%) completed their neoadjuvant therapy. Only 198 (50%) returned for definitive pathologic restaging, and 149 (37%) underwent thoracotomy for attempted resection. Predictors of who returned to the surgical arena were age (< 70), multiple node involvement, and response to neoadjuvant therapy. The 5-year survival was 8% for the 253 patients who did not return for restaging but was 47% for the 149 patients who underwent thoracotomy (p < 0.001). The 5-year survival for selected subgroups of patients who underwent complete resection was 42% for the 14 patients who had unsuspected recalcitrant N2 disease, 49% for the 65 patients who had a partial response, and 53% for the 34 patients who had a complete response.
Conclusions: Only 37% of patients with favorable, nonbulky, biopsy-proven N2 disease actually complete their neoadjuvant therapy, undergo restaging, and then return for attempted resection. Only 28% undergo complete resection. However, in this highly selected subset of patients, the 5-year survival is 47% or better if partial or complete pathologic response is achieved. Therefore, surgical resection remains a viable treatment for selected patients with favorable N2 NSCLC.
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Introduction |
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Many studies on N2 disease feature patients who are staged by many different physicians, are clinically staged only and have not undergone biopsies to prove N2 disease, have bulky as well as microscopic N2 disease, and use inconsistent treatment algorithms [2, 3]. In some studies patients are only staged using computed tomography (CT) scans with 10-mm columinated cuts, without contrast. They then go directly for surgical resection, and only one or two N2 lymph nodes are sampled. Some patients with N2 disease have obvious but "ignored N2 disease" and still go on to resection, whereas others have careful preoperative staging and have "unsuspected, "nonimaged," or "integrated positron emission tomography (PET)/CT negative" or "surprise" N2 disease.
This study examined a large number of patients with a very similar type of N2 disease. It used integrated PET/CT as well as CT scans using 5-mm columinated cuts along with intravenous contrast. In addition, patients underwent selective mediastinoscopy, endoscopic transesophageal ultrasound with fine needle aspirate (EUS-FNA), and endoscopic transbronchial ultrasound-guided FNA (EBUS) of mediastinal N2 lymph nodes.
All patients had consistent and thorough clinical and pathologic staging before operation, all had biopsy-proven N2 disease, underwent similar N2 and M1 staging procedures and similar neoadjuvant therapy protocols, and then had similar restaging tests and operations. One physician performed the clinical and pathologic staging, as well as the operations. Most important, all patients had nonbulky N2 disease initially. This limits many of the confounding variables seen in other studies as described above.
The purpose of this study was to identify the results of a homogenous group of patients who were carefully staged and who had biopsy-proven, favorable N2 disease in order to identify characteristics of who retuned to the surgical arena. In addition, we wanted to compare the different survival rates for the different groups of patients after neoadjuvant chemoradiotherapy.
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Material and Methods |
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Entry and Exclusion Criteria
Patients who underwent mediastinoscopy and had bulky N2 disease that was fixed to mediastinal structures such as the trachea were excluded from this study. Also excluded were patients who had more than one mediastinal N2 lymph node that was 2.5 cm or greater who did not undergo mediastinoscopy but who had biopsy-proven N2 disease by EUS-FNA or by EBUS. Thus, only patients with nonbulky or nonfixed N2 disease, or both, were included in this study. Patients with N2 disease in more than one N2 station were candidates for this study if none of the lymph nodes were bulky or fixed as defined above. Patients with biopsy proven N3 disease were also excluded. Any patient who had received previous radiation or chemotherapy, or both, for an earlier NSCLC, who had N3 disease, or who had radiation or chemotherapy based solely on clinical staging (ie, it was not biopsy-proven N2 disease) were excluded from this study.
The University of Alabama at Birmingham's Institutional Review Board approved this study as well as the electronic prospective database that was used. Individual patient consent was obtained for entry in the prospective database but was waived for inclusion in this study.
Staging
Staging was performed as previously described [5]. In brief, patients were pathologically staged after being clinically staged using PET scan or integrated PET/CT and CT scan. All suspicious N2, N3, or M1 locations, defined after PET as areas with a maximum standardized uptake value (maxSUV) exceeding 2.5, underwent biopsy before pulmonary resection. Mediastinoscopy was used to biopsy suspicious lymph nodes in the paratracheal area (stations 2R, 4R, 2L, 4L, and top of 7), and EUS [6] was used to biopsy suspicious left-sided paratracheal lymph nodes (4L), subcarinal (7), periesophageal (8), and inferior pulmonary ligament nodes (9). Mediastinoscopy was not routinely used in all patients; however, if CT or PET suggested N2 or N3 disease, mediastinoscopy was performed if EBUS or EUS-FNA was negative. In addition, mediastinoscopy was also used for patients without evidence of N2 or N3 disease if the primary lung tumor was 4 cm or greater, centrally located, or if tumors had a maxSUV on PET of 10 or greater. EUS-FNA was performed as previously described [7].
The "clinical stage" and "pathologic stage" were defined using the criteria of the International Union Against Cancer/American Joint Committee on Cancer (UICC/AJCC) [4, 8]. To be more even more specific, we further defined "clinical stage" into two types. The first term, "clinical stage after radiologic staging only," was defined as the stage as suggested after CT and integrated PET/CT scans were performed. The second term, "clinical stage after minimally invasive mediastinal lymph node biopsies," was defined as the stage after mediastinoscopy, EBUS, or EUS-FNA, or both, were all completed. Finally, pathologic stage was defined as the stage after thoracotomy, resection of the tumor, and complete thoracic lymphadenectomy were performed.
Pathologic review was performed using standard techniques, and immunohistochemical staining was used when appropriate. A final pathologic stage was then generated by using the T, N, and M classification system according to the international staging system [4]. Pathologic response was defined as complete (T0 N0 M0), partial (T1-T4 N0 or T1-T4 N1), and nonresponder (T1-T4 N2, T1-T4 N3, or T1-T4 N2-N3 M1). The term "recalcitrant or persistent" N2 disease refers to a patient having N2 disease initially, undergoing neoadjuvant chemoradiotherapy, and then having N2 disease in the same lymph node location. An "R0 resection" was defined as complete resection of the entire tumor with negative margins and with removal of all thoracic mediastinal lymph nodes.
Restaging
All patients who were diagnosed with N2 disease underwent platinum-based chemotherapy, and nearly all also received radiation treatment. Most patients received radiation doses of 60 Gy or higher [9]. Patients underwent repeat FDG-PET and CT scans 1 month after the completion of their neoadjuvant therapy. After restaging studies, patients who were fit for operation and who had an initially positive EBUS or EUS-FNA result of an N2 lymph node underwent a repeat procedure with rebiopsy of the same lymph node that was previously malignant. Repeat mediastinoscopy was not performed, and thus EBUS or EUS-FNA, or both, were used to rebiopsy the appropriate lymph node station that was initially positive for N2 disease if an initial mediastinoscopy was positive.
Statistics
Analysis was conducted using SAS 9.0 software (SAS Corp, Cary, NC). Continuous data are presented as medians, and categoric data are presented as percentages. The Fisher exact test or Pearson 
2 test was used to assess categoric data and the Wilcoxon test to evaluate continuous variables. Survival estimates were derived by Kaplan-Meier analysis, and Mantel-Haenszel log-rank tests were used to assess differences in survival amongst groups. Cox proportional hazards stepwise modeling was used to investigate and adjust for major prognostic factors. A two-sided value of p < 0.05 was considered statistically significant and unlikely due to chance. All variables in the univariate analysis with p < 0.10 were entered into the stepwise multivariable model.
Patients alive or free of disease at the end of the study period, or at the end of the follow-up period, were censored for purposes of data analysis. Death from any cause was used to determine the overall survival rate.
Follow-up consisted of chest and abdominal CT scans every 6 months for the first 2 years and yearly afterwards. The final data acquisition point was January 2007, and patients were followed up from June 1997 to September 2007. Data were obtained from multiple sources such as clinic letters, follow-up scans, hospital computer information systems, tumor registry, Social Security Death Index, telephone calls, and letters from oncologists and other physicians. All information was entered into our prospective database.
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Results |
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As reported in Table 3, the overall 5-year survival of the 402 patients in this study was 13.2%. Table 3 also summarizes 5-year survival of several subsets of study patients. The 5-year survival was only 4.8% for the 39 patients who did not even complete their neoadjuvant therapy and was only 17% for those who did finish it but did not come for resection. The lower portion of Table 3 reports results for three favorable and distinct groups of patients who did undergo R0 resection. The 5-year survival was 42% for the 14 patients who had unsuspected recalcitrant N2 disease, 49% for the 65 patients who had a partial response, and 53% for the 34 patients who had a complete response.
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Comment |
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The standard of care for N2 disease is extremely controversial. Recently, the American Association of Chest Physicians (AACP) published its evidence-based clinical practice guidelines for NSCLC. Interestingly and controversially, the guidelines stated, "in NSCLC with N2 disease identified preoperatively (IIIA) induction therapy followed by surgery is NOT recommended except as part of a clinical trial" [10]. In addition, they also state, "for NSCLC patients with N2 disease identified preoperatively (IIIA) platinum-based combination chemoradiotherapy is recommended as the primary treatment" [10].
In our institution, as well as in others, neoadjuvant high-dose chemoradiotherapy is the preferred treatment for patients with favorable (nonfixed and nonbulky) N2 disease who may be candidates for surgical intervention after therapy. Hence, this was the entry criteria for inclusion into this study, and this fact must be remembered when the results of this study are interpreted. Our study therefore considers a more favorable and homogenous group of patients with N2 disease than previous reports on stage IIIA N2 disease [11, 12]. Our patients had nonbulky, mobile, or nonfixed N2 disease, or a combination, were all considered potentially operable, and were sent for consideration of neoadjuvant therapy. In our practice, patients with bulky N2 lymph nodes or those with N2 lymph nodes that are fixed to surrounding mediastinal structures are generally not considered for surgical resection after their chemoradiotherapy is finished.
Furthermore, it is important to note that we have increased our preoperative dose of radiation from the more common and standard dose of 45 Gy to higher or curative doses of 60 to 70 Gy [13]. The reason for this is to maximize the effectiveness of the radiation therapy and to prevent gaps in the completion of radiation treatment if after restaging the patient has recalcitrant N2 disease and does not undergo surgical resection. Thoracotomy and pulmonary resection is safe after these high doses of preoperative radiation if intercostal muscle flaps are used to buttress the irradiated bronchus [14]. These caveats must all be remembered when interpreting this study's findings.
Even though this study was restricted to patients with a more favorable type of N2 disease, we found that only 81% completed their planned preoperative chemoradiotherapy and only 198 (50%) of these remaining patients returned for definitive surgical restaging. Only 149 of these 198 patients (39%) went on to thoracotomy and attempted resection, and of the 149 who underwent resection, only 113 (28%) underwent R0 resection. Therefore, of the initial 402 patients with biopsy-proven favorable N2 disease, only 113 truly finished our planned course of action, which was biopsies to prove N2 disease and rule out N3; neoadjuvant high-dose chemoradiotherapy, followed by pathologic restaging; and then complete resection. These results surprised us. Obviously during this period, other patients who had unfavorable N2 disease were seen at our institution and were never sent for surgical consideration. They are not included in this study, but their survival would most likely be worse.
There are several reasons why patients did not return for definitive surgical (pathologic) restaging. The most common was a lack of response to therapy. Another reason was morbidity that occurred during the neoadjuvant therapy that precluded resection. A third reason was that some patients were told their tumors had "progressed," but yet never had definitive biopsies to prove this assumed progression after restaging tests were preformed. These patients did not return to see the surgeon and often went on to second-line chemotherapy after restaging tests, despite the lack of pathologic proof of progression. In 2005 we showed the inaccuracies of staging tests despite integrated PET/CT and the use of 5-mm cut CT scan for the initial staging of patients with NSCLC, and it is likely that these tests also harbor inaccuracies for restaging after chemoradiotherapy [15].
We found predictors of who returned to the surgical arena for resection were younger age (< 70 years), single N2 lymph node station involvement, and response to neoadjuvant therapy. Patients who returned for attempted curative resection enjoyed a significantly greater survival than those who did not.
Another important finding of this study was the survival in certain subgroups of patients who underwent complete R0 resection after the completion of their neoadjuvant chemoradiotherapy. These survival data, although impressive must be kept in the context of the overall survival for the 402 patients in this series of only 13% and of the caveats and selection criteria of this study that were described. The 5-year survival was 53% for the 34 patients who had a complete pathologic response and 49% for the 65 patients with a partial response. Even more surprising was the 5-year survival of 42% for the 14 patients who had recalcitrant N2 disease and had R0 resection. In 2003 Barlesi and colleagues [16] reported a 5-year survival rate of 0% for 20 patients who had recalcitrant N2 disease and who underwent complete resection. In contrast, Lorent and colleagues [17] in 2004 reported a 4-year survival rate of 50%. In 2006 Jaklitsch and colleagues [2] reported a 5-year survival of 18% for patients with recalcitrant N2 disease in the Cancer and Leukemia Group B (CALGB 8935) study.
These vastly different survival rates for patients with the same stage disease are explained by the disparate entry criteria of the different studies. Most of these studies included patients with bulky N2 disease, and not all patients had R0 resection. These factors are quite different than our entry criteria. Our high survival for patients with recalcitrant N2 disease who underwent complete resection was based on the highly select group of patients who had resection:
Thus, although these 14 patients all had "recalcitrant N2 disease on final path," it is a different type of recalcitrant N2 disease than is described in other studies.
On the basis of all of our findings from this study, we have presented our recommended treatment strategy for patients with N2 disease, which is shown in Figure 3. As depicted in that figure, we do not recommend thoracotomy and resection for known recalcitrant N2 disease, but may consider it in selected patients who are young, have evidence of response of the primary tumor and of the affected lymph node (decrease in the size and in the maximum standardized uptake values on integrated PET/CT of both), and who can undergo R0 resection with lobectomy or bilobectomy.
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Recalcitrant or persistent N2 disease after neoadjuvant chemoradiotherapy is usually a contraindication for resection. However, in a very select groups of patients who have evidence that their N2 nodes have been down-staged after repeat EUS-FNA or repeat EBUS, or both, and who undergo complete R0 resection but turn out to have unsuspected microscopic recalcitrant N2 disease, a 5-year survival of 42% may be achievable. Surgical resection may be a reasonable option for these patients, but caveats for offering resection in this highly select group of patients seem to be the primary tumor and the entire N2 nodal disease can undergo an R0 resection by lobectomy (not pneumonectomy), patients are young with good pulmonary function and performance status, and they do not have multilevel N2 disease initially before induction chemoradiotherapy.
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Discussion |
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I have a couple of comments and then two questions for you specifically. One of the comments is that these results are outstanding, but also, Cerf, astounding. They go in the face of data that we have from individual institutions, like the Brigham that were presented by Dr Jaklitsch, and they go in the face of every one of the phase II and phase III trials so far for trimodality therapy in that you have basically shown us that even in patients who don't have a pathologic complete response, you, Dr Cerfolio, can achieve a 50% 5-year survival in stage III resected lung cancer.
DR CERFOLIO: Hard to believe, isn't it?
DR KRASNA: It is.
DR CERFOLIO: I agree with you, the survival was hard for me to believe as well, especially for those with recalcitrant N2 disease.
DR KRASNA: I'll get to that as my first question. How can you explain the difference between your findings and everyone else's, including our own?
My other question, though, I think perhaps to elucidate for all of us to better understand your subset, because we did see the diminishing denominator, exactly how did you restage the patients? I understood from Lee the number of patients who underwent initial surgical vs EUS [endoscopic transesophageal ultrasound] lymph node staging, but how did you actually restage those patients after they had the CT [computed tomography] or the CT-PET [positron emission tomography]? In other words, how many patients had surgical restaging prior to your thoracotomy, or were these all findings at thoracotomy?
I actually want to end with a comment, which is that I do believe that it is important to identify that there is a subset of these stage III patients who will benefit from surgery, but you will have to clarify for us how you got there. Thank you.
DR CERFOLIO: First of all, I appreciate your comments. I would like to thank Lee, who is a first-year medical student and did this project as a college student. He has a histology test. I appreciate him coming and presenting this data so well. [Applause.] So, Lee, you can get on an airplane and go back and take your tests now and relax, it is over.
Now, to answer your questions, Dr Krasna, I agree with you. In fact, when I saw the survival, especially of the patients who had recalcitrant N2 disease that I took out of the talk because even I don't believe it is so high, you have to ask yourself how, but Ayesha Bryant, who we all know well, went back and very carefully reviewed all our survival and it is accurate. So then, if the data are accurate, how can it be so high? Well I think you hit the nail on the head when you stated that this is a very select group of patients. Remember, the overall survival for the 400 patients was only about 10%, which is even worse than some of those studies you quoted earlier. So, this is a very highly selected group of patients.
So the message is not, oh, if someone has recalcitrant N2 disease, go ahead and resect them. The message is only 1 out of 4 patients with N2 disease even come back to resection, and then of those with pathologic recalcitrant or persistent N2 disease, it was N2 disease that was negative on restaging EUBS [endoscopic transbronchial ultrasound-guided] or EUS-FNA [fine needle aspiration] after chemoradiotherapy, but positive only on pathology probably because I took the whole node out at the time of surgery, and it was carefully reviewed by the pathologists and in some cases immunohistochemical staining was used. We are highly selecting those who had recalcitrant N2 disease to get it, and almost all of them are pathologic recalcitrant N2.
To answer your second question now, everybody who had a positive EUS got a repeat EUS. Everybody who had a positive mediastinoscopy got an EUS or an EBUS, or both, which we started much later in this series, after the completion of chemoradiation. We have just been doing that for a year. So we didn't do a repeat mediastinoscopy. Everybody also got a repeat PET. So we went after every suspicious node. If the node was initially positive, we rebiopsied it, and if it was suspicious somewhere else, we biopsied it.
Having said that, you saw how many patients we didn't take to the OR [operating room] because they had recalcitrant N2 disease. Then if you find this very subset of patients that look like they have been down-staged, we then operated on them, and even at the time of surgery, if we found nodes that looked suspicious, we would take them out, and in some patients, stop. You saw the number that went to the OR that we didn't resect.
So the take-home message is that the vast majority of people who have N2 disease don't come back to the OR and don't do that well, with a survival of 13%; but a highly select group of patients who are young, who have a very good response to the primary tumor, that their lymph nodes shrinks on CT and the FDG [fluorodeoxyglucose] avidity goes down by 70%, may benefit from surgery. On final path there still may be cancer there, they are still IIIA, they are still recalcitrant N2, but they have gone from macroscopic N2 to microscopic N2 only, and they do well and they undergo lobectomy. Their tumors can be completely resected with lobe; however, I do not recommend resecting them with recalcitrant N2 if it requires a pneumonectomy. I hope this explains why the survival is hard for even me to believe, and they are my patients.
DR TIMOTHY M. ANDERSON (Boston, MA): Cerf, once again, congratulations on an excellent paper. At the time of mediastinoscopy, how certain are you that fixed disease to the mediastinum or so-called frozen mediastinum is a contraindication to neoadjuvant therapy? Secondly, these patients once diagnosed with N2 disease in a way become condemned, if you will, to neoadjuvant therapy. Could you tweak out a subset of those patients who may have had central tumors, pneumonias, or tumor bleeding who might have died or become rendered inoperable during the earlier chemotherapy arm of neoadjuvant therapy that might have been better off getting surgery, followed by adjuvant therapy? In other words, do you foresee a shift in the paradigm from neoadjuvant to adjuvant therapy for selected IIIa disease patients?
DR CERFOLIO: Good questions. I do not think IIIA in general—we all know it is very heterogeneous disease—is best treated by surgery and adjuvant therapy. I think it is a marker for systemic disease.
To answer your second question first, we are going to be presenting tomorrow on a highly selected group of patients with unsuspected microscopic N2 disease, and those are the ones I think that if you resect and they get adjuvant chemo do pretty well, but I don't have any data that if you gave them neoadjuvant chemo up front followed by surgery, compared to surgery followed by adjuvant therapy, that they may have done even better had we done it pre-op. I don't know. So that's the answer to your second question.
Your first question, this, again, was a highly selected group of patients initially because they had N2 disease that was mobile. I would disagree with you, if you were saying that patients with fixed N2 disease, that is gross and with enlarged lymph nodes with capsular invasion, should be treated with surgery up front. When I see someone with bulky 2R and 4R and a bulky number 7 wrapped around the trachea or the right upper lobe bronchus with a 3-cm right upper lobe mass, who is not a patient that I really think I am ever going to bring back to the OR, no matter how much radiation and chemo they get, I tell them I'll see them back and I am happy to consider it, but it is unlikely they will undergo resection.
DR MALCOLM M. DECAMP (Boston, MA): Can you comment on the difference between response and restaging? I assume your responders were identified by typical size criteria, greater than 50% reduction in the cross-sectional diameter, etc, and that is often very different than what you find by repeat EUS, repeat EBUS, repeat PET, maxSUV [maximum standardized uptake value], or even what you find at the time of surgery. Can you comment on how you defined response?
DR CERFOLIO: That is an excellent question, because, again, that self-selects this group and it is why the survival is so high. That definition was pathologic definition. The vast majority of these patients were EUS-positive at number 7, got radiation and chemo, the CT scan showed the node got smaller, the maxSUV of that number 7 lymph node went down by 20% or 30% or more, the patients then all got re-EUS-FNA'd, they were now pathologically negative, I then took them to the OR, did a right upper lobectomy, took the No. 7 lymph node out, and lo and behold, there is some microscopic recalcitrant N2 disease. So they would be listed as a partial responder, but they are recalcitrant N2, but we all know that they had a very good response, and hence, the high survival numbers seen in this study. I think this example is quite typical of many of the patients in this series.
DR JOEL D. COOPER (Philadelphia, PA): Great paper. It addresses the question that all of us want to know, which is have we come into the era of operating on N2 disease where surgery may be an adjuvant. The 5-year survival that you gave was about 10% of the patients you started with. Is that correct?
DR CERFOLIO: That's about right.
DR COOPER: And some of those were complete responders. So it still raises the question, of all the patients you started with, if you had not operated on any of them vs chemorads, and that is an essential question when faced with the patient before they start down the pathway. I would just like your comments on that.
Also, a 5-year survival depends on what your mean follow-up is. How many patients have actually crossed the 4-year or 5-year time frame in terms of your survival curve? It is a great paper—a very important issue—and I appreciate the presentation very much.
DR CERFOLIO: Thank you. The median follow-up was 3.7 years for the 402 patients in the study. So a large number of patients crossed the 5-year threshold. That's number one. Number two, your first point is really the key, and actually, as usual, I go into these studies with an opinion and my opinion is often wrong when I look at the data. And that happened in this study: My opinion was wrong. I have been telling patients in my clinic for probably 7 years: "Oh, your mediastinoscopy is positive but only in one node and it is mobile so although this is a problem, don't worry. You're going to get radiation and chemotherapy. You have a 50% chance of coming back and I'm going to resect you," but when you look at my own data, that speech I have been giving them is wrong: Only about 25% come back for surgery. So the vast majority really don't come back to surgery, the vast majority really don't do well, and these were people that I thought really didn't have fixed N2.
So, Dr Cooper, I think your point is right on the button. It is still a bad predictor and the role of surgery still is controversial and remains to be seen. I think the ACCP guidelines are a little bit too much the other way—that there is no role for surgery for IIIA—and I don't agree with that, but I think we have to tease out the select group of patients that do benefit from surgery.
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