Quality of Life Following Lung Cancer Resection - CHEST Journal

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Key words: lung cancer; quality of life; thoracotomy; video-assisted thoracic surgery. Abbreviations: EORTC. European Organization for Research and Treatment ...
Quality of Life Following Lung Cancer Resection* Video-Assisted Thoracic Surgery vs Thoracotomy Wilson W. L. Li; T. W. Lee, MB, ChB; Shirley S. Y. Lam, RN; Calvin S. H. Ng, MBBS (Hons); Alan D. L. Sihoe, MB, BChir; Innes Y. P. Wan, MB, ChB; and Anthony P. C. Yim, MD, FCCP

Study objectives: Quality of life (QOL) following video-assisted thoracic surgery (VATS) major lung resection has not been systematically studied. This study was designed to evaluate the intermediate to long-term QOL in patients with lung cancer following resection, comparing VATS with thoracotomy. Design: Cross-sectional study, telephone survey. Methods: Of 136 disease-free surviving patients with non-small cell lung cancer operated on between 1994 and 2000, 45 patients were excluded because of large tumors (> 5 cm) or locally advanced disease, and another 27 patients were excluded because of adjuvant therapy, coexisting cancer from another source, or psychiatric illness. At the time of the survey, 13 patients were found to be either unsuitable or unwilling to participate. This left a total of 51 patients, with 27 patients in the VATS group and 24 patients in the thoracotomy group (open group), for the final analysis. QOL was assessed using Chinese versions of the European Organization for Research and Treatment of Cancer (EORTC) Quality of Life Questionnaire (QLQ)-C30 and the EORTC QLQ-LC13, supplemented with nine self-developed surgery-related questions. Results: Mean follow-up time was 33.5 months in the VATS group (median, 20.8 months; range, 6.0 to 84.2 months) and 39.4 months in the open group (median, 37.7 months; range, 7.0 to 75.1 months). Both groups had good QOL and high levels of functioning despite a fairly high incidence of symptoms. There was a trend for VATS patients to score higher on the QOL and functioning scales and to report fewer symptoms. However, these differences did not lead to statistical significance. Conclusions: This study showed that lung cancer patients with resectable disease following surgical treatment without recurrence have good QOL and high levels of functioning on intermediate to long-term follow-up, with no significant differences between the VATS and open groups. (CHEST 2002; 122:584 –589) Key words: lung cancer; quality of life; thoracotomy; video-assisted thoracic surgery Abbreviations: EORTC ⫽ European Organization for Research and Treatment of Cancer; NSCLC ⫽ non-small cell lung carcinoma; QLQ ⫽ Quality of Life Questionnaire; QOL ⫽ quality of life; VATS ⫽ video-assisted thoracic surgery

urgical resection continues to be the mainstay of S treatment for early non-small cell lung carcinoma (NSCLC).1 Traditionally, this is done through a thoracotomy. However, with the introduction of minimal access techniques, major pulmonary resections can now be performed with video-assisted thoracic surgery (VATS). *From the Division of Cardiothoracic Surgery, Department of Surgery, The Chinese University of Hong Kong, Prince of Wales Hospital, Hong Kong SAR, China. Manuscript received September 21, 2001; revision accepted March 18, 2002. Correspondence to: Anthony P. C. Yim, MD, FCCP, Professor and Chief, Division of Cardiothoracic Surgery, Department of Surgery, The Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, NT, Hong Kong SAR, China; e-mail: [email protected] 584

The fact that access trauma is lessened in VATS has been well documented. Studies on lobectomy comparing VATS with thoracotomy have suggested that the former is associated with short-term benefits such as decreased postoperative pain,2–5 decreased perioperative morbidity,4 –7 better postoperative pulmonary function,8,9 reduced length of hospital stay,3,6,10 lower hospital costs5,10 and earlier return to normal activities.3,11 However, the effect of these early benefits on the patient’s long-term quality of life (QOL) remains uncertain. With the building evidence that survival after VATS lobectomy is similar to the survival after lobectomy by thoracotomy,5– 8,12 QOL assessments become increasingly important in the evaluation of these treatClinical Investigations

ment options. Sugiura et al11 attempted to assess the long-term QOL in lung cancer patients after lobectomy, comparing VATS (n ⫽ 20) with thoracotomy (n ⫽ 15); they suggested that VATS lobectomy was associated with improved long-term QOL. However, they used a limited questionnaire containing only six questions. No studies have been undertaken to our knowledge on postoperative long-term QOL in patients undergoing VATS using standardized questionnaires. We conducted a cross-sectional study to assess the intermediate to long-term QOL in patients with early NSCLC after major lung resection, comparing VATS with the standard posterolateral thoracotomy approach, the results of which form the basis of this publication. Materials and Methods Patients All surviving patients with resectable NSCLC who underwent surgical resection at the Prince of Wales Hospital, Hong Kong, between March 1994 and October 2000, with no evidence of recurrence were considered for this study. All patients underwent surgery at least 6 months previously. One hundred thirty-six patients were initially regarded as potential candidates. In order to make both groups comparable, patients with tumor size ⬎ 5 cm or locally advanced tumor requiring extended resection were excluded from the study (n ⫽ 45), as these patients would not be candidates for VATS. Patients who received adjuvant therapy (n ⫽ 14) or had other forms of cancer (n ⫽ 11) or psychiatric illness (n ⫽ 2) were also excluded from the study. At time of the telephone survey, two patients were hospitalized for stroke and were unable to participate. Three patients were unavailable for follow-up, and six patients were unable to understand the questionnaires due to old age or senile dementia. Two patients refused to participate in the study. As a result, a total of 51 patients were available for analysis, including 27 patients who underwent VATS lobectomy (VATS group) and 24 patients who underwent lobectomy by thoracotomy (open group). Operative Technique Our technique for VATS lobectomy has been described in detail elsewhere.2,7 We emphasize on avoiding rib spreading and torquing of the thoracoscope at all times. For open lobectomy, we perform the standard posterolateral thoracotomy with division of the latissimus dorsi and serratus anterior muscles. QOL Assessment QOL was assessed using three different questionnaires: the Chinese version of the European Organization for Research and Treatment of Cancer (EORTC) Quality of Life Questionnaire (QLQ)-C30 (cancer core questionnaire), the Chinese version of the EORTC QLQ-LC13 lung cancer-specific questionnaire module, and a self-developed module containing nine additional surgery-related questions. The questionnaires were sent to the patients, accompanied by a letter with general information and aim of the study. All QOL data were collected thereafter by a trained research nurse through telephone interviews. In order to avoid bias, the operating surgeons were not involved at any point in the questioning. www.chestjournal.org

EORTC QLQ-C30 The EORTC QLQ-C30 (version 3.0) is a self-rating questionnaire composed of 30 questions/items and incorporates nine multi-item scales: five functional scales (physical, role, cognitive, emotional, and social), three symptom scales (fatigue, pain, nausea/vomiting), a global health/QOL scale, and several single items assessing additional symptoms (dyspnea, sleep disturbance, constipation, and diarrhea). A final item evaluates the perceived economic consequences of the disease. Reliability and validity of the English and Chinese versions of the EORTC QLQ-C30 questionnaire have been confirmed in international studies.13–15 EORTC QLQ-LC13 The EORTC QLQ-LC13 is a supplemental questionnaire module that was designed for use among patients receiving treatment with chemotherapy and/or radiotherapy. It contains 13 questions/items assessing lung cancer-associated symptoms (cough, hemoptysis, dyspnea, and site-specific pain), chemotherapy/radiotherapy-related side effects (sore mouth, dysphagia, peripheral neuropathy, and alopecia), and pain medication. The dyspnea scale was aggregated into a four-item scale by including the single dyspnea item of the EORTC QLQ-C30 core questionnaire.16 Chemotherapy/radiotherapy-related side effects were not included in the analysis. Reliability and validity of the EORTC QLQ-LC13 module have been confirmed in international studies.15,16 Additional Questions No lung cancer surgery-specific module has as yet been developed for use with EORTC questionnaires. In order to develop such a module, a lung cancer surgical treatment literature review was undertaken and discussions were held with cardiothoracic surgeons. Main lung cancer surgery-related problems are dyspnea, shoulder dysfunction, scar problems, and thoracotomy pain. Dyspnea is sufficiently covered by combining the EORTC QLQ-C30 and EORTC QLQ-LC13 into one dyspnea scale, as described in a previous study.16 Therefore, we produced a series of questions to assess the patient’s shoulder function, scar problems, thoracotomy pain, and their effect on the patient’s QOL. An additional question was added to assess the overall satisfaction with the surgical procedure. The selfdeveloped questions were modified into nine questions/items (Table 1) after testing in a pilot study with 24 patients. The items have the same format and scale scoring as the EORTC QLQ-C30 and EORTC QLQ-LC13 and employ the same time frame. The

Table 1—Self-Developed Lung Cancer Surgery-Related Questions Supplemented to the EORTC QLQ-C30 and EORTC QLQ-LC13 1. Have you had any difficulty using your arm or shoulder on the side of the chest operation? (scale 1–4) 2. Did the above-mentioned situation interfere with your daily activities? (scale 1–4) 3. Has the scar interfered with your family life? (scale 1–4) 4. Has the scar interfered with your social activities? (scale 1–4) 5. Have you had any pain in or around the scar? (scale 1–4) 6. Have you had numbness in or around the scar? (scale 1–4) 7. Did climatic changes affect the feeling of the scar? (scale 1–4) 8. Did the scar pain interfere with your daily activities? (scale 1–4) 9. What is your overall impression about the operation? (scale 1–7)

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nine items are classified into three multi-item symptom scales assessing shoulder dysfunction, scar problems, and postthoracotomy pain; one final single item assesses the overall satisfaction with the surgical procedure. Statistical Analysis Statistical analysis was performed using statistical software (Statistical Package for the Social Sciences for Windows, version 10.0; SPSS; Chicago, IL). All scores of the EORTC QLQ-C30 and EORTC QLQ-LC13 and additional questions were linearly transformed so that all scales range from 0 to 100. For the global health/QOL and functioning scales, higher scores represent a higher level of functioning. For the symptom scales, higher scores represent a greater degree of symptoms. The proportion of patients who have a specific symptom is defined as the percentage of patients who reported a symptom scale scoring ⬎ 0. Results are reported as mean, SD, and frequency. QOL data were compared using the Mann-Whitney U test; frequencies were compared using a ␹2 test. If an expected frequency in at least one cell of the table in the ␹2 test is ⬍ 5, the Fisher exact test was computed instead. Spearman rank-correlation coefficient was used to examine correlations between variables. A two-tailed p ⬍ 0.05 was considered statistically significant. The reliability of the multi-item scales was assessed using Cronbach ␣ coefficient for internal consistency. Cronbach’s ␣ coefficient ⬎ 0.5 signals acceptable reliability, while Cronbach’s ␣ coefficient ⬎ 0.7 was considered good reliability.

Results Fifty-one patients were recruited for the study, and their characteristics are shown in Table 2. There are 27 patients in the VATS group and 24 patients in the open group. There were no significant differences between the two groups in age, sex, education level, marital status, or follow-up period. Mean follow-up time was 33.5 months in the VATS group (median, 20.8 months; range, 6.0 to 84.2 months) and 39.4 months in the open group (median, 37.7

Table 2—Demographic Data of the Study Populations* Variables Age, yr Sex Male Female Marital status Single Married Divorced/separated Widowed Education level None Primary school Secondary school University Follow-up, mo

VATS Group (n ⫽ 27)

Open Group (n ⫽ 24)

63.0 ⫾ 14.7

66.6 ⫾ 13.7

20 (74.1) 7 (25.9)

18 (75.0) 6 (25.0)

2 (7.4) 20 (74.1) 0 (0.0) 5 (18.5)

3 (12.5) 16 (66.7) 0 (0.0) 7 (29.2)

7 (25.9) 13 (48.1) 7 (25.9) 0 (0.0) 33.5 ⫾ 27.7

7 (29.2) 9 (37.5) 5 (20.8) 3 (12.5) 39.4 ⫾ 24.1

p Value NS NS

NS

NS

NS

*Data are presented as mean ⫾ SD or No. (%). NS ⫽ not significant. 586

months; range, 7.0 to 75.1 months). Pathologic data are described in Table 3. All patients successfully completed the questionnaires. All questionnaires were well understood, including the nine self-developed items. Mean scores and SDs of the EORTC QLQ-C30 and EORTC QLQ-LC13 functioning and symptom scales, and selfdeveloped QOL scales are shown in Tables 4, 5. Both groups reported high satisfaction with the surgical procedure. Also, both the VATS group and the open group reported good QOL and high levels of functioning overall, despite a fairly high incidence of reported symptoms (Tables 4, 5). The most frequently reported symptoms were fatigue, coughing, dyspnea, and thoracotomy pain. There was a trend for VATS patients to score higher on the QOL and functioning scales and to report fewer symptoms. Furthermore, patients undergoing VATS tended to take less pain medication. However, of all the functioning and symptom scales, only the constipation scale showed significant difference (p ⬍ 0.001) in favor of patients undergoing VATS. All EORTC multi-item scales showed at least acceptable reliability (Table 6). Furthermore, the Cronbach ␣ coefficients for the three self-developed multi-item QOL scales showed good reliability as well. Discussion In our study, we found that our patients undergoing VATS and thoracotomy enjoyed good QOL and Table 3—Pathologic Data and Surgery Performed* Variables Tumor histology Adenocarcinoma Squamous cell carcinoma Large cell carcinoma Other Tumor size, cm TNM classification T1N0M0 T2N0M0 T1N1M0 T2N1M0 T3N0M0 Lobectomies performed RUL RML RLL RUL and RML RML and RLL LUL LLL

VATS Group (n ⫽ 27)

Open Group (n ⫽ 24)

17 (63.0) 4 (14.8) 0 (0.0) 6 (22.2) 2.5 ⫾ 1.1

11 (45.8) 6 (25.0) 4 (16.7) 3 (12.5) 3.1 ⫾ 1.3

15 (55.6) 11 (40.7) 0 (0.0) 1 (3.7) 0 (0.0)

9 (37.5) 11 (45.8) 1 (4.2) 2 (8.3) 1 (4.2)

6 (22.2) 0 (0.0) 6 (22.2) 0 (0.0) 0 (0.0) 8 (29.6) 7 (25.9)

8 (33.3) 1 (4.2) 1 (4.2) 1 (4.2) 2 (8.3) 10 (41.7) 1 (4.2)

*Data are presented as No. (%) or mean ⫾ SD. RUL ⫽ right upper lobe; RML ⫽ right middle lobe; RLL ⫽ right lower lobe; LUL ⫽ left upper lobe; LLL ⫽ left lower lobe. Clinical Investigations

Table 4 —EORTC QLQ-C30 and QLQ-LC13 Scores in Lung Cancer Patients After Surgery* VATS Group (n ⫽ 27) Variables Functioning scales† Physical Role Emotional Cognitive Social Global QOL† Symptom scales/items‡ Fatigue Nausea/vomiting Pain Insomnia Appetite loss Constipation Diarrhea Financial difficulties Dyspnea Coughing Hemoptysis Pain in chest Pain in arm or shoulder Pain in other parts



Mean ⫾ SD

Open Group (n ⫽ 24) %§

87.2 ⫾ 13.5 90.7 ⫾ 16.2 83.6 ⫾ 21.0 84.6 ⫾ 16.6 90.1 ⫾ 17.5 65.4 ⫾ 18.3 74 15 67 41 15 22 26 44 85 82 7 48 59 37

23.9 ⫾ 20.1 4.9 ⫾ 14.5 17.9 ⫾ 17.9 18.5 ⫾ 25.0 6.2 ⫾ 16.1 7.4 ⫾ 14.1 12.3 ⫾ 22.9 19.8 ⫾ 24.9 24.7 ⫾ 18.0 38.3 ⫾ 27.3 2.5 ⫾ 8.9 18.5 ⫾ 21.4 22.2 ⫾ 20.7 17.3 ⫾ 25.1

92 21 71 54 33 71 21 46 75 75 8 29 46 54

Mean ⫾ SD

p Value㛳

85.8 ⫾ 10.6 86.1 ⫾ 18.8 76.7 ⫾ 22.5 77.1 ⫾ 21.3 81.3 ⫾ 20.4 56.6 ⫾ 22.1

NS NS NS NS NS NS

31.5 ⫾ 19.0 6.9 ⫾ 14.7 19.4 ⫾ 19.5 27.8 ⫾ 28.9 11.1 ⫾ 16.1 31.9 ⫾ 26.9 6.9 ⫾ 13.8 23.6 ⫾ 31.8 23.3 ⫾ 18.4 34.7 ⫾ 25.0 2.8 ⫾ 9.4 12.5 ⫾ 21.6 19.4 ⫾ 23.9 23.6 ⫾ 26.9

NS NS NS NS NS ⬍ 0.001 NS NS NS NS NS NS NS NS

*See Table 2 for expansion of abbreviation. †Scores range from 0 to 100. Higher scores represent higher levels of functioning or QOL. ‡Scores range from 0 to 100. Higher scores represent higher levels of symptoms or problems. §Percentage of patients who reported a symptom score ⬎ 0. 㛳 p value refers to Mann-Whitney U test testing for differences in medians; means are given for informative purposes.

high levels of functioning after a mean follow-up of 3 years. VATS patients tended to score higher on QOL and functioning scales and reported relatively fewer symptoms. However, comparison of these scales did not reveal any significant differences. Particular attention has been paid in this study to the incidence of long-term pain. This was assessed with the EORTC pain scales, supplemented with our selfdeveloped thoracotomy pain scale, which combined the scores of questions on pain and numbness

in and around the scar, along with effects of climatic changes. A large percentage of both groups of patients still reported some degree of pain (VATS group, 74%; open group, 75%; Table 5). However, the reported mean scores for pain were low, with no significant differences found between the two groups. Furthermore, there was no significant difference regarding the current use of pain medication. However, it was interesting to see that constipation was the only significantly different symptom among

Table 5—Reported Scores of the Self-Developed Lung Cancer Surgery-Related Questions in Lung Cancer Patients After Surgery* VATS Group (n ⫽ 27)

Open Group (n ⫽ 24)

Variables



Mean ⫾ SD



Mean ⫾ SD

p Value㛳

Symptom scales/items† Shoulder dysfunction Scar problems Thoracotomy pain Satisfaction with surgery‡

33 19 74

13.6 ⫾ 21.2 4.9 ⫾ 11.1 19.1 ⫾ 18.0 84.0 ⫾ 24.2

33 29 75

11.8 ⫾ 19.3 7.6 ⫾ 13.0 21.2 ⫾ 18.9 82.6 ⫾ 19.3

NS NS NS NS

*See Table 2 for expansion of abbreviation. †Scores range from 0 to 100. Higher scores represent higher levels of symptoms or problems. ‡Scores range from 0 to 100. Higher scores represent higher satisfaction with surgery. §Percentage of patients who reported a symptom score ⬎ 0. 㛳 p value refers to Mann-Whitney U test testing for differences in medians; means are given for informative purposes. www.chestjournal.org

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Table 6 —Multi-item Scale Reliability (Cronbach ␣ Coefficients) Variables EORTC QLQ-C30 Physical functioning Role functioning Emotional functioning Cognitive functioning Social functioning Global QOL Fatigue Nausea/vomiting Pain EORTC QLQ-LC13 LC dyspnea EORTC QLQ-C30 (item 8) Self-developed scales Shoulder dysfunction Scar problems Thoracotomy pain

Items

VATS Group (n ⫽ 27)*

Open Group (n ⫽ 24)*

1–5 6, 7 21–24 20, 25 26, 27 29, 30 10, 12, 18 14, 15 9, 19

0.70 0.71 0.89 0.77 0.79 0.92 0.84 0.91 0.71

0.56 0.93 0.86 0.74 0.54 0.94 0.85 0.89 0.51

3–5 ⫹

0.80

0.80

1, 2 3, 4 5–8

0.92 0.84 0.73

0.79 0.81 0.62

*Cronbach ␣ coefficient ⬎ 0.5 signals acceptable reliability; Cronbach’s ␣ coefficient ⬎ 0.7 is considered good reliability.

the two groups. This could be related to a difference in the overall use of analgesia after surgery. Our findings seem to be consistent with some reported studies. Nomori et al17 recently reported no significant differences between their VATS group and an anterior thoracotomy group for lung cancer resection in terms of postoperative respiratory muscle strength, 6-min walk test, and pain scores after 2 weeks. However, it should be noted that in their VATS group, rib spreading was used.18 Landreneau et al19 studied the prevalence of chronic pain and pain-related morbidity after pulmonary resection comparing VATS with thoracotomy; they found that VATS is associated with reduced pain and shoulder dysfunction during the first year after surgery. However, no significant differences could be found after a year follow-up. Dales et al20 studied prospectively the QOL in lung cancer patients following surgical resection through thoracotomy; they found that QOL deteriorated in the first 3 months after surgery but returned to preoperative levels at 6 to 9 months. Similar findings were reported by Zieren et al21 in a more recent study. Possible QOL benefits of VATS are therefore likely to be maximal up to 9 months postoperatively. However, Sugiura et al11 attempted to assess the long-term QOL in lung cancer patients following surgery comparing VATS with thoracotomy; they found that VATS was associated with long-term QOL benefits. However, a limited, nonvalidated questionnaire was used in this study that contained only six questions. Furthermore, there was a significant difference in follow-up time (VATS, 12.6 months; thoracotomy, 33.6 months; p ⫽ 0.0001), making comparison less valid. 588

We acknowledge that our present study has several limitations. First of all, our findings are limited by the small sample size. This is a critical point in our investigation, calling for cautious conclusions at this stage. If QOL benefits exist for VATS patients after long-term follow-up, they are likely to be small. Therefore, with our current sample size, these differences are less likely to be found statistically significant. Furthermore, due to the cross-sectional design of the study, randomization or collection of QOL data at baseline was not possible. To adjust for the lack of randomization, selection criteria for the study were strict in order to reduce the number of possible confounding factors that could have affected the two groups’ preoperative and postoperative QOL besides their difference in surgical approach. Crosssectional studies still yield valuable information, but the dynamic characteristics of QOL are best assessed in a longitudinal setting. However, in the absence of preoperative baseline assessments, we cannot determine whether VATS and thoracotomy patients have comparable preoperative data, or whether we are instead studying two groups of patients with different initial levels of QOL. Future studies need to be prospective, longitudinal and should include larger study populations. And finally, although we used standardized questionnaires to assess QOL, the reliability and validity of the EORTC questionnaires have been confirmed in stage III and IV lung cancer patients only.13–16 It is unknown whether these standardized questionnaires are also applicable to early lung cancer patients. Regarding our selfdeveloped questionnaire, psychometric analysis revealed high Cronbach ␣ coefficients for the three self-developed surgery related multi-item symptom Clinical Investigations

scales (Table 6), suggesting a high level of construct validity and an adequate grouping of the selfdeveloped item scales. However, these questions are used for the first time and may require more extensive validation. Further studies are needed to assess the psychometric properties of this lung cancer surgery-specific QOL questionnaire module in the current groups of patients. To our knowledge, this study represents a first step in documenting intermediate to long-term QOL in lung cancer patients following surgery using standardized and validated questionnaires. Despite the mentioned limitations and the lack of statistically significant findings, our findings offer valuable information. Major advantages of the VATS procedure should be found mainly in the early postoperative period. Therefore, equal performance regarding QOL11 and length of survival5– 8,12 after long-term follow-up would already justify the application of VATS for the resection of early stage lung cancers. In conclusion, we found in this cross-sectional study that lung cancer patients, following surgical treatment through either VATS or thoracotomy with intermediate to long-term follow-up without recurrence, enjoy good QOL and high levels of functioning. Although VATS patients tended to score higher on the QOL and functioning scales and reported relatively fewer symptoms, there were no significant differences. Prospective randomized studies with long-term follow-up would be warranted to confirm these findings, which we are currently undertaking. ACKNOWLEDGMENT: The authors thank Professor Benny C. Y. Zee, PhD, and Tony S. K. Mok, MD, for thoughtful input.

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