Gen Thorac Cardiovasc Surg (2014) 62:112–118 DOI 10.1007/s11748-013-0340-3

ORIGINAL ARTICLE

Stage II–IV lung cancer cases with lymphovascular invasion relapse within 2 years after surgery Satoshi Shiono • Naoki Kanauchi • Naoki Yanagawa Masami Abiko • Toru Sato



Received: 19 August 2013 / Accepted: 24 October 2013 / Published online: 2 November 2013 Ó The Japanese Association for Thoracic Surgery 2013

Abstract Objective For recurrent lung cancer, postoperative follow-up methods have not been adequately assessed, and no evidence-based postoperative surveillance methods currently exist. Herein, we evaluated postoperative lung cancer recurrence and the personalized postoperative surveillance periods and methods used. Methods Follow-up after surgery consisted of a regular outpatient clinic check-up, including physical examination, history, blood tests, and chest X-ray, which were conducted three or four times per year for 5 years. During the followup period, annual chest and brain computed tomography scanning was performed. Between May 2004 and December 2011, 547 lung cancer patients underwent complete resection in our institution. We retrospectively reviewed their prospectively collected data. Results We selected 106 patients (19.4 %) who had a postoperative recurrence. Multivariate analysis showed that advanced stage (stage II–IV; p \ 0.01) and lymphovascular

Presented at the 65th Annual Scientific Meeting of the Japanese Association for Thoracic Surgery, Fukuoka, Japan, October 17 to October 20, 2012. S. Shiono (&)  M. Abiko  T. Sato Department of Thoracic Surgery, Yamagata Prefectural Central Hospital, 1800, Oazaaoyagi, Yamagata 990-2292, Japan e-mail: [email protected] N. Kanauchi Department of Thoracic Surgery, Nihonkai General Hospital, Sakata, Japan N. Yanagawa Departments of Pathology and Laboratory Medicine, Yamagata Prefectural Central Hospital, Yamagata, Japan

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invasion positivity (LVI; p = 0.01) were independent risk factors for earlier recurrence. Overall, 90.8 % of patients with advanced-stage disease and LVI positivity experienced a relapse within 2 years after surgery, compared to 55.1 % of patients who did not have these factors (p \ 0.01). Multivariate analysis showed that recurrence with symptoms (p \ 0.01) and shorter time to recurrence (\24 months; p \ 0.01) were independent prognostic factors after recurrence. Conclusions Although this study was retrospective and included some biases, patients with advanced-stage lung cancer and LVI positivity should be intensively followed up. Personalized follow-up programs should be considered for lung cancer patients who have undergone resection. Keywords

Lung cancer  Surgery  Recurrence

Introduction Lung cancer is the leading cause of cancer death worldwide. While advances in diagnosis, surgery, and perioperative chemotherapy have provided better outcomes, about 30 % of patients who undergo complete lung cancer resection experience disease recurrence [1–4]. Even patients with stage I disease may develop recurrence [5, 6]. Postoperative recurrence survival (PRS) is poor. Sugimura reported that in 445 lung cancer cases who relapsed after surgery, the median PRS was 8.1 months [2]. Most lung cancer recurrences develop in distant organs [7]. Locoregional recurrence of clinical stage I non-small cell lung cancer (NSCLC) has been reported to develop in\10 % of cases who undergo lobectomy, 8–25 % of cases who undergo segmentectomy, and 17–55 % of cases who undergo wedge resection [8].

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Whether earlier detection of lung cancer recurrence can improve patient outcomes is not well understood. Advances in radiographic treatment modalities and chemotherapy have enabled physicians to achieve better outcomes for postoperative lung cancer recurrence. Yet, the optimal timing of treatment for recurrence and a role for postoperative surveillance have not been fully explored. Although some guidelines include recommendations for postoperative follow-up, no definitive recommendations for the optimal postoperative follow-up period or methods exist [9– 11]. Recently, the risk of recurrence has been suggested to depend on the individual status of each patient, suggesting that postoperative follow-up should be personalized [12]. The objective of this study was to investigate the tendency of recurrence and to identify prognostic factors for postoperative recurrence in patients undergoing lung cancer surgery. Therefore, the endpoint of this study was recurrence after surgery. Furthermore, to address the possibility of a personalized follow-up method after lung cancer surgery, we evaluated lung cancer patients who developed recurrences; data were collected prospectively and investigated retrospectively.

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contiguously anatomical site, including the ipsilateral hemithorax and mediastinum, after surgical resection. Distant recurrence was defined as tumor recurrence in the contralateral lung or outside the hemithorax and mediastinum after surgical resection. The follow-up schedule consisted of a visit with thoracic surgeons 1 or 2 weeks after surgery and every month thereafter for up to 3 months. When no problems were noted, follow-up was performed by thoracic surgeons or physicians every 3–4 months for 5 years. Regular outpatient clinic check-ups, including physical examination, history, blood chemistry, serum tumor markers, and chest X-ray were performed three to four times a year for 5 years. During the follow-up period, annual chest and brain CT with or without contrast-enhanced material was conducted. Among patients who were followed for 5 years, surviving patients continued to be followed with chest X-ray or CT. During the follow-up period, if the patient presented with symptoms, these radiological studies, as well as PET/CT, bone scintigraphy, and/or brain magnetic resonance imaging (MRI) were performed. Beginning in Table 1 Patient characteristics and risk factors

Materials and methods Our institution has established a prospective database of patients who have undergone lung cancer; this database was updated for this study. Since positron emission tomography/computed tomography (PET/CT) was available starting in May 2004, this retrospective study was performed from that time to December 2011. During the study period, 566 patients underwent lung cancer surgery at our institution. Cases with incomplete resection, cases with asynchronous or metachronous multiple lung cancers, and patients who died of any cause within 30 days after surgery were excluded from the present study. Additional data that were necessary to establish the database were abstracted from medical records. Lung cancer staging followed the TNM staging method (TNM Classification of Malignant Tumors, 7th Edition) [13]. We also recorded the date of recurrence, signs used to detect recurrence, symptoms associated with recurrence, methods used to find recurrence, treatments administered after recurrence, date of last follow-up, date of death, and cause of death. When recurrences were found by imaging, the date of imaging was considered to be the date of recurrence. A multidisciplinary team made the final diagnosis of recurrence. If a biopsy was feasible and available, pathological confirmation was performed. The differential diagnosis of pulmonary metastasis or secondary lung cancer was based on the martini and melamed criteria [14]. Local recurrence was defined as tumor recurrence in a

Variables

n (%)

Mean age, years (range)

69 (47–83)

Gender Male/female

76 (66)/30 (34)

Smoking history ±

75 (71)/31 (29)

Median CEA (ng/mL)

3.6 (0.6–129.5)

SUV index

4.8 (0–12.0)

Surgery Non-limited/limited

92 (87)/14 (13)

Pathology Ad/non-ad

58 (55)/48 (45)

P-stage IA/IB/IIA/IIB/IIIA/IV

24 (23)/23 (22)/18 (17) /10 (9)/30 (28)/1 (1)

LVI ±

47 (44)/59 (56)

Detection of recurrence FU/symptoms

68 (64)/38 (36)

Treatment ±

87 (82)/19 (18)

EGFR-TKI ±

17 (16)/89 (84)

Distant mets. ±

77 (73)/29 (27)

CEA carcinoembryonic antigen, SUV standardized uptake value, SUV index tumor SUV max/liver SUV mean, LVI lymphovascular invasion, FU follow-up, EGFR-TKI epidermal growth factor receptor tyrosine kinase inhibitor

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114

October 2007, evaluation of epidermal growth factor receptor (EGFR) mutation status was routinely conducted on paraffin-embedded materials. Survival was analyzed with the Kaplan–Meier method. Cox proportional hazards modeling was used in univariate and multivariate analyses to evaluate the risk factors associated with postoperative recurrence. Time to recurrence was defined as the time from surgery to a first diagnosis of recurrence. PRS was defined as the time from the first diagnosis of recurrence to death or the date of last follow-up. Patients without PRS events were censored at the time of the last clinical visit. Data were analyzed with version 5.0.1 of the JMP software package (SAS Institute Inc., Cary, NC, USA). Statistical significance was assigned to p values of \0.05. The Ethics Committee of our institution approved this study and waived the need for informed consent as long as patient data remained anonymous.

Gen Thorac Cardiovasc Surg (2014) 62:112–118

recurrences were detected during the following types of follow-up surveillance: CT (n = 41), elevated tumor marker (n = 15), chest X-ray (n = 7), physical examination (n = 3), PET/CT (n = 1), and bronchofiberscopy (n = 1). Sixty-eight patients (64 %) were found to have a recurrence during follow-up surveillance, and 38 patients (36 %) were found to have a recurrence based on symptoms; these symptoms included pain (n = 12), neurological symptoms (n = 6), cough (n = 6), fatigue (n = 4), dyspnea (n = 3), hemosputum (n = 2), and other (n = 5). Risk factors for early recurrence after surgery The median time to recurrence was 12 months (1–72 months). Cumulative recurrence rates after surgery were 53 % at 1 year, 81 % at 2 years, and 98 % at 5 years. Univariate analysis was used to investigate the relationships between time to recurrence and possible risk factors. As seen in Table 2, male gender, smoking status, non-

Results Distribution of patients with recurrence Of the 566 surgical lung cancer patients, 37 patients with multiple lung cancers, 18 patients with incomplete resection, and 1 patient with incomplete data were excluded; 510 patients could thus be evaluated. No patient died within 30 days of surgery. We selected 106 patients (19.4 %) who had a postoperative recurrence for analysis of associations between recurrence and clinical factors. With respect to pathological stage, 24 of 257 (9.3 %) patients with stage IA disease, 23 of 115 (20.0 %) patients with stage IB disease, 18 of 61 (29.5 %) patients with stage IIA disease, 10 of 25 (40.0 %) patients with stage IIB disease, 30 of 50 (60.0 %) patients with stage IIIA disease, and 1 of 2 (50.0 %) patients with stage IV disease developed a recurrence. Patients had a median follow-up period of 65 months (range 9–98 months). Table 1 summarizes the characteristics of the study population. Recurrence developed at the following sites: regional lymph node (n = 37), lung (n = 32), bone (n = 17), brain (n = 17), pleura (n = 7), liver (n = 5), surgical margin (n = 5), adrenal gland (n = 4), and other (n = 6). Overall, 4 of 14 (28.6 %) patients who underwent wedge resection or segmentectomy and 25 of 92 (27.2 %) patients who underwent non-limited resection developed local recurrence only; this difference was not statistically significant (p = 0.91). A total of 78 of 106 (82 %) patients received treatment for lung cancer recurrence, including chemotherapy (n = 50), radiotherapy (n = 22), chemoradiation (n = 9), and surgery (n = 6); 19 patients received best supportive care. In 68 patients (64 %),

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Table 2 Univariate analysis of recurrence and risk factors for recurrence Variables

Median time to recurrence (M)

Hazard ratio (95 % CI)

p

12/10

1.14 (0.92–1.41)

0.23

13/12

0.77 (0.61–0.96)

0.02

12/18

1.31 (1.06–1.64)

0.01

10/12

1.02 (0.82–1.26)

0.85

11/14

1.16 (0.94–1.44)

0.17

12/12

0.93 (0.72–1.27)

0.64

14/10

0.77 (0.63–0.94)

\0.01

10/16

1.38 (1.10–1.63)

\0.01

10/15

1.36 (1.12–1.66)

\0.01

12/12

0.59 (0.86–1.28)

0.59

12/12

0.98 (0.80–1.20)

0.83

Age, years ]75/\75 Gender F/M Smoking ± CEA (ng/mL) [5/^5 SUV index

a

[5/^5 Surgery Non-limited/limited Pathology Ad/non-Ad Stage II–IV/I LVI ± Postop. adj ± Detection of rec. FU/symptoms

CI confidence interval, CEA carcinoembryonic antigen, SUV standardized uptake value, SUV index tumor SUV max/liver SUV mean, Ad adenocarcinoma, LVI lymphovascular invasion, postop. postoperative, adj adjuvant therapy, rec. recurrence, FU follow-up a

SUV data for 18 patients were not available

Gen Thorac Cardiovasc Surg (2014) 62:112–118

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Table 3 Multivariate analysis of recurrence and risk factors for recurrence Variables

Hazard ratio (95 % CI)

p

Gender F

Table 4 Univariate analysis of prognostic factors for PRS and PRS Prognostic factors

3-year PRS

Hazard ratio

95 % CI

p

]75

29

10.4

1.38

1.05–1.78

0.02

\75

77

33.7 0.65–1.10

0.20

0.90–1.59

0.24

0.99–1.02

0.21

1.07–1.89

0.02

0.69–1.41

0.80

0.50–0.83

\0.01

1.04–1.74

0.02

0.88–1.46

0.31

0.53–0.89

\0.01

0.41–0.77

\0.01

0.44–1.05

0.09

Age, years 0.98 (0.69–1.38)

0.92

Smoking ?

n

1.41 (0.99–2.04)

0.06

Gender Male

76

23.6

0.84

Ad

0.93 (0.73–1.18)

0.57

Female

30

37.5

1

Stage II–IV

1.34 (1.08–1.66)

\0.01

Smoking ?

Pathology

LVI ?

– 1.33 (1.07–1.65)

75

25.7

1.18

31

33.5

1

0.01

CEA

CI confidence interval, Ad adenocarcinoma, LVI lymphovascular invasion

[5

35

11.7

1.01

^5

71

33.6

1

SUV indexa [5

43

17.5

1.41

^5

45

41.4

1

Non-limited

92

24.9

0.96

Limited

14

33.3

1

Ad

58

43.1

0.69

Non-ad

48

12.4

1

59

16.0

1.34

47

41.6

1

Surgery

Pathology

P-stage II–IV I LVI ?

47

21.2

1.14



59

33.5

1

FU

68

35.6

0.69

Symptoms

38

13.5

1

Detection of rec.

Fig. 1 Comparison of recurrence in patients with advanced stage and LVI-positive cancer with recurrence in those who do not have these factors

adenocarcinoma histology, advanced stage, and lymphovascular invasion (LVI) positivity were risk factors for a shorter time to recurrence. Next, multivariate analysis was performed to identify the independent factors that were significant in the univariate analysis. Since the standardized uptake value (SUV) data for 18 patients were not available, these cases were excluded from the multivariate analysis. Multivariate analysis revealed that advanced stage and LVI positivity were independent significant factors for earlier recurrence (Table 3). As shown in Fig. 1, 90.8 % of patients with LVI-positive advanced-stage disease experienced disease recurrence within 2 years after surgery, compared to 55.1 % of patients who did not have these factors (p \ 0.01).

Treatment ?

87

31.8

0.55



19

0

1

EGFR-TKI ?

17

46.0

0.71



89

25.0

1

77 29

27.1 30.6

1.08 1

0.83–1.44

0.57

]24 months

20

61.9

0.52

0.30–0.78

\0.01

\24 months

86

20.6

1

Distant mets. ? – Time to rec.

PRS postoperative recurrence survival, CI confidence interval, CEA carcinoembryonic antigen, SUV standardized uptake value, SUV index tumor SUV max/liver SUV mean, Ad adenocarcinoma, LVI lymphovascular invasion, rec. recurrence, FU follow-up a

SUV data for 18 patients were not available

123

116

Gen Thorac Cardiovasc Surg (2014) 62:112–118

Table 5 Multivariate analysis of prognostic factors for PRS and PRS Prognostic factors

Hazard ratio

95 % CI

p

1.01

0.75–1.35

0.94

0.79

0.60–1.05

0.11

1.22

0.94–1.61

0.14

0.66

0.50–0.87

\0.01

0.62

0.44–0.89

0.01

0.52

0.30–0.80

\0.01

Age, years ]75 Pathology Ad P-stage II–IV Detection of rec. FU Treatment ? Time to rec. ]24 months

CI confidence interval, SUV standardized uptake value, Ad adenocarcinoma, FU follow-up, rec. recurrence, PRS postoperative recurrence survival

Survival and prognostic factors after recurrence Among patients who experienced disease recurrence, the 5-year survival rate after surgery was 31.6 %, and median survival was 26 months (range 4–92 months). Overall survival rates after recurrence were 61.1 % at 1 year, 40.2 % at 2 years, 27.8 % at 3 years, and 9.0 % at 5 years; median overall survival was 16 months (range 0–78 months). At last follow-up, 40 patients were alive, 61 patients had died of lung cancer, and 3 patients had died of other causes. The outcomes of 2 patients are unknown. Univariate analysis revealed that age, SUV index, non-adenocarcinoma histology, advanced stage, recurrence with symptoms, no treatment, and shorter time to recurrence (\24 months) were prognostic factors for PRS (Table 4). Table 5 shows the results of multivariate analysis, which revealed that recurrence with symptoms, no treatment, and shorter time to recurrence (\24 months) were independent prognostic factors for PRS.

Discussion A large-scale study by Taylor et al. [4] showed that a high PET SUV, preoperative radiotherapy, and pathological stage II and III disease were associated with recurrence. Interestingly, in a subgroup analysis, sublobar resection was associated with locoregional recurrence, and LVI was associated with distant metastasis. The present study revealed that patients with advanced-staged disease and LVI developed recurrence earlier, within 2 years of surgery. According to the concept of recurrence dynamics for

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NSCLC, peaks of recurrence occur at 9 months, 2 years, and 4 years after surgery [15]. It appears that lung cancer recurrence does not occur in a simple fashion. Yoshino et al. [16] reported a 2-year PRS rate of 15.7 %, Lou et al. [17] reported a 3-year PRS rate of 24 %, and the present study demonstrated a 3-year PRS rate of 27.8 %. Symptoms, low performance status (PS), neoadjuvant chemotherapy, adjuvant radiotherapy, recurrence sites, and treatment were associated with PRS [2]. Multivariate analysis by Endo et al. [3] showed that male gender, pleural invasion, extrathoracic recurrence, and supportive care for recurrence were associated with poor outcome. Yoshino et al. [16] reported that female gender, early p-stage, younger age at recurrence, metastasectomy, and intra-pulmonary metastasis were significant favorable factors in patients with distant metastases. Nakagawa et al. [18] showed that cervico-mediastinal and liver metastases also decreased survival. In the present study, multivariate analysis revealed that recurrence with symptoms, no treatment for recurrence, and shorter time to recurrence (\24 months) were significantly associated with poor prognosis after recurrence. Walsh et al. [19] revealed that the median survival duration from the time of recurrence was 8.0 months for symptomatic patients and 16.6 months for asymptomatic patients (p = 0.008). Although these findings might reflect the efficacy of postoperative followup, they could not exclude a lead-time bias. Since our results may also include a lead-time bias, they should be interpreted carefully. In this study, we explored the possibility of personalized postoperative follow-up. Our study showed that 90.8 % of patients with advanced and LVI-positive lung cancer relapsed within 2 years after surgery, compared to 55.1 % of patients without these factors (p \ 0.01). To treat recurrences earlier, high-risk patients should be followed up intensively, while other patients can be followed less intensively, even just 2 years after surgery. Some studies were unable to detect any differences in outcomes between patients who underwent intensive versus nonintensive follow-up [19–21]. Westeel et al. [22] reported that an intensive surveillance program of routine bronchoscopy and thoracic/abdominal CT was feasible. Optimal follow-up modalities are controversial. Although no randomized trials have compared chest CT to X-ray, CT is considered to be better for detecting lung cancer recurrence [11, 18, 23]. In the present study, recurrences were found in 41 of 106 (39 %) patients by CT. Korst et al. [24] demonstrated sensitivity and specificity values of 94 and 87 %, respectively, for CT in making a diagnosis of recurrence, although the positive predictive value was low (55.3 %). Lou et al. [17] reported that follow-up after curative resection for lung cancer by routine CT

Gen Thorac Cardiovasc Surg (2014) 62:112–118

identified 93 % of new primary cancers and 61 % of recurrences. Chiu et al. [25] revealed the utility of lowdose CT in the surveillance of lung cancer recurrence in a small study. Recent guidelines have recommended CT during post-treatment follow-up [9–11, 23], suggesting that the role of follow-up chest CT will become increasingly important. As there are many problems to clarify in postoperative follow-up after lung cancer surgery, prospective randomized studies are needed. Because this was a small, retrospective, single-institution study, the statistical power was not sufficient to make universal conclusions; this is the major limitation of our study. In addition, lead-time bias could not be excluded. A final limitation is the lack of second lung cancer cases. Generally speaking, diagnosis of second lung cancers is very difficult. Due to this, we only investigated obvious pulmonary metastasis of lung cancer in this study.

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7.

8.

9.

10.

11.

12.

Conclusion

13.

In conclusion, we have demonstrated that postoperative lung cancer recurrence, particularly for advanced and LVIpositive lung cancers, tends to occur within 2 years. These patients should be intensively followed up. Personalized follow-up programs should, therefore, be considered for lung cancer patients who undergo resection. Acknowledgments this study.

We received no funding or financial support for

Conflict of interest

None.

14. 15.

16.

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Stage II-IV lung cancer cases with lymphovascular invasion relapse within 2 years after surgery.

For recurrent lung cancer, postoperative follow-up methods have not been adequately assessed, and no evidence-based postoperative surveillance methods...
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